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Edred John Henry Corner, 1972. 
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THE GARDENS’ BULLETIN 
SINGAPORE 


TROPICAL BOTANY 


Essays presented to 


E. J. H. Corner 
for his seventieth birthday, 1976 


Compiled and edited by 


D. J. MABBERLEY and CHANG KIAW LAN 


Published by Authority 


Issued by the Commissioner, Parks and Recreation Department 


Printed by the Singapore National Printers (Pte) Ltd 


1977 


To be purchased at the Botanic Gardens, Singapore 


Price: $$30.00 


CONTENTS 


H. M. BurxILu: Introduction - - - . : : 
D. J. MaBBERLEY: E. J. H. Corner’s Botany - - ‘ : 


William T. STEARN: The of gis gaia’, imme With Sa a: 
Vegetation 


P. S. AsHTon: Ecology and the Durian Theory — - ‘ E 


E. SoepapMo & B. K. Eow: hai Roa Per ~— 
zibethinus Murr. - 


Frances M. JARRETT: The ne of Artocarpus — a unique binloniels 
phenomenon - - - a a : F 


D. J. MABBERLEY: The Origin . the fap abies ai Flora and 
its Implications - . M ‘ 


Frank WHITE: The fintier ida Forests of Africa: A preliminary 
review - - - - - - - - 


B. L. Burtr: Notes on Rain-Forest Herbs sz : if 7 


E. F. Bkunic & H. KLINGE: Comparison of the Phytomass Structure 
of Equatorial ‘‘Rain-Forest” in Central Amazonas, Brazil, and in 
Sarawak, Borneo - - - - - - 


C.G.G.J. VAN STEENIS: Autonomous Evolution in Plants: differences 
in plant and animal evolution - i A : 


Andrey A. FEporov: On Speciation in the Humid Tropics: some 
new data - - - - - - - - 
Benjamin C. STONE: The Morphology and SS i ni of Pandanus 
Today (Pandanaceae) - - - - 
Hsuan KENG: Ternstroemia corneri (Theaceae) - - - : 
R. E. HoLtruM: Thelypteridaceae Allied to Phegopteris in Malaya - 


A. Davip & M. JAQUENOUD: Tremellales with Tubular Hymenophores 
Found in Singapore - : . . : : ‘ 


Jacqueline PERREAU & RoGeR HeEIM: Sur Un Nouveau Bolet Tropical 
a Spores Ornées~ - - - ‘ i . : 


A. FAHN & D. M. JoEL: Development of Primary Secretory Ducts in 
the Stem of Mangifera indica L. (Anacardiaceae) - - - 


Kenneth R. SporNe: Girdling Vascular Bundles in Dicotyledon 
Flowers - - . _ ; z P ; 


F. HALLE & D. J. MABBERLEY: Corner’s Architectural Model - - 


Robert F. THORNE: Where and When Might ¥e Trop Ansa 
mous Flora Have Originated? . - 


J. GALIL, M. STEIN & A. Horovitz: On the en of the SCORES 
Fig (Ficus sycomorus L.) in the Middle East - - 


J. T. Wiepes: A Short History of Fig Wasp Research - - : 
V. H. Heywoop: The Taxonomist’s Dilemma - : : . 


D. G. FRoDIN: On the Style of Floras: some general considerations —- 
Edwin A. MENNINGER: This World We Live in Will Be Only as 

Beautiful as You and I Make It - - - : - 
Index - - - . 
Errata - . , “ ; 


PAGE 
12 
s-11 


13-18 
19-23 


25-33 


35-39 


41-55 — 


57-71 
73-80 
81-101 
103-126 
127-136 


137-142 
143-144 
145-150 


151-153 
155-160 
161-164 


165-173 
175-181 


183-189 


191-205 
207-232 
233-237 
239-250 


251-253 
255-266 
266 


THE 


GARDENS BULLETIN 
SINGAPORE 


Vol. XXIX 31st August, 1977 


Introduction 
H. M. BurKILL 


Royal Botanic Gardens, Kew 
(Botanic Gardens, Singapore, 1954-1969) 


Corner’s septuagenary fell on 12 January, 1976, It was the intention of a number of 
his research students and friends to develop an idea mooted by David Frodin into a little 
book to mark the occasion. However. 


‘The best-laid schemes o’ mice an’ men 
Gang aft a-gley, 
And lea’e us nought but grief an’ pain 


For promised joy.’ 
(Robert Burns: To a mouse, 1785.) 


Very considerable difficulties have arisen over the preparation and publication, so that 
only now, by the courtesy of the Editor of the Gardens’ Bulletin, Singapore, does it appear 
— in retrospect, but, nevertheless, in a token of our esteem. 


It was but inevitable that with such innate stimulating enthusiasm for botany, Corner 
should find the opportunity during his service in Singapore to give free rein to it. The 
‘Durian Theory’ of evolution is here discussed, as along with the tropical rain-forest which 
Corner demonstrated in his later years as Professor of Tropical Botany at Cambridge ought 
to form the central pillar of any basis for teaching botany. Universities in tropical regions 
in centres of floral evolution with the plant materials on their door-step should be mindful 
of establishing leading research schools instead of letting the world rely on botanists tutored 
on temperate botany. Long before announcing his Durian Theory but with perhaps the seeds 
of the idea quietly growing in his mind, Corner began teaching, amongst his other duties 
in the Botanic Gardens, students in the Raffles College and in the King Edward VII 
College of Medicine in Singapore. These are now integral parts of the University of 
Singapore, and many of the older collegiates recall his lectures with interest and pleasure. 


In 1937 while on expedition in N.E. Malaya he brought a young berok monkey (Macaca 
nemestrina). This is the species that is trained to pick ripe coconuts, and Corner saw the 
possibility of training one to pick plant specimens from high forest trees at a height of 
perhaps 50-60 m from the ground. The berok had its début on a trip to Fraser’s Hill and 
proved to be so successful that two more were acquired, and later a fourth. Words of a 
command had to be taught to guide the monkey to what was wanted visible to the operator 
lying on the ground scanning the tree-canopy through binoculars. Infinite patience was 
necessary, and both he and his assistant, Ngadiman bin Haji Ismail, often suffered painful 
monkey-bites. Closer to Singapore, the Mawai-Sungei Sedili swamp-forest, accessible on 
single-day forays, was an area of much interest to Corner, and the monkeys were often used 
there. To ‘those-in-the-know’, this area is called Corner’s Corner, and it was here that 
he contracted a disease akin to black-water fever that very nearly killed him, an end 
frustrated by skilled and devoted nursing in the Singapore General Hospital, At that time 
the only access to Kuala Sedili was by river from Mawai. Now the time-conscious and 
hurry-mad swoosh down to the river-mouth by highway and agricultural settlement has 
pushed back very large tracts of the drier forest, and has chased out the elephants, tigers 
and wild-life that I have been fortunate enough to see there. But the actual swamp-forest, 
by virtue of its wetness, still has a life-expectancy (who knows?) for many years till 


l 


2 Gardens’ Bulletin, Singapore — X XIX (1977) 


‘development’ demands further rapine. So it is good to learn that Corner has written 
an account of the Southern Malayan swamp forests that he knows so well and that his 
account is soon to appear as a supplement to the Gardens’ Bulletin, Singapore. 


Under a growing conciousness for conservation of biological resources, nature reserves 
were created in Singapore in 1937 and were put under the Gardens control. Ngadiman 
was Head Ranger and the team of monkeys were daily exercised there when they were not 
out on expedition. Thus Corner had constant interest in the reserves, especially the Bukit 
Timah Reserve where the use of the monkeys added to our knowledge of the tree flora. 
The mangrove reserve at Pandan was patrolled by an honorary warden, the late Towkay 
Chua Ho Ann, who was allowed to take a limited amount of timber for charcoal burning 
as guid pro quo for replanting and his wardenship. During the Japanese occupation Chua 
had a big charcoal contract with the Japanese Navy and consequently was ‘in the money.’ 
Both Holtum and Corner were retained by the Japanese in an advisory capacity in the 
Gardens, and Chua was able to pass not inconsiderable sums of money over to Corner 
which he used for the benefit of Gardens staff on the black market. During the latter part 
of this time, he and Holttum lived in a single room in the Botanic Gardens Director’s 
house which was my study while I lived there. Corner, it seems, liked to ‘live dangerously.’ 
Contact with outside persons was not allowed and the receipt of money, had it been dis- 
covered, would have had the most serious consequences. Furthermore, Japanese Military 
Officers lived upstairs and their radio had its attractions and risks. 


When Singapore surrendered to General Yamashita in 1942, the arrival of Professor 
Hidezo Tanakadate rescued the Botanic Gardens from military occupation. Sir Shenton 
Thomas, as former Governor of the Straits Settlements, had written a letter requesting the 
Japanese authorities to respect libraries, scientific collections, and places of historic interest. 
This letter Corner gave to Tanakadate who, with his own high influence and a long friend- 
ship with the General from student days, combined the Botanic Gardens and Raffles Museum 
into a unit of conservation. Presidency of this unit was accepted by Marquis Tokugawa, 
Supreme Consulting Adviser to the Nippon Military Administration, and this organisation 
received the personal approval of Count Terauchi, Supreme Commander of S.E, Asia. On 
the return of Tanakadate to Tokyo, Professor Kwan Koriba took charge of the Botanic 
Gardens, He was assisted by K. Watanabe who, in Singapore and Penang, assembled a 
remarkable collection of drawings of economic plants. In 1945 the drawings were deposited 
for safety in the Singapore herbarium. In 1960 Watanabe asked if they might be returned 
to him for publication, but they could not be found. Then blew an ill wind. In 1963 the old 
herbarium was in danger of collapse; its contents were hurriedly removed, and the drawings 
came to light. There followed an encyclopaedic work of reference prepared jointly by 
Corner and Watanabe: Illustrated Guide to Tropical Plants (1969). 


Of the early days, Dr. Furtado, of the Gardens Staff, recalls a matter of interest and 
importance that is worth recording. Corner foresaw looting and persuaded the authorities to 
have officially signed notices of prohibited entry to the Raffles Library, the Raffles College 
and the building of the offices of the law firm Donaldson and Burkinshaw in which lay the 
largest private collection of lawbooks. Corner personally drove Tanakadate in the Gardens 
lorry to fix up these decrees. Equipment and the books of these buildings were thus saved 
from looting and damage. Count Terauchi also directed the valuable books from the 
Government House Library to be stored in the Tanglin Barracks. Corner was also able 
to salvage parts of the library of the Colonial Secretariat in Empress Place which had been 
thrown out of the building. At the end of the war when the Allied Forces entered Singapore 
Corner was again instrumental in obtaining similar protection from the British Military 
Administration, and though the Garden became a tented campsite no unauthorised entry 
was made into the buildings. 


During these difficult years both Corner and Holttum, free from administrative duties, 
were able to devote much time to research. Corner worked on the larger fungi; and the 
development of flowers and fruits of various families of trees, The monograph on Clavaria, 
as indeed also, the Durian Theory began to take shape at this time, and in the post war 
years we have seen with admiration a succession of major works that must have had their 
origins in adversity. But this period had made a mark: he was invalided out of service in 
1947, though happily he was soon to regain good health, and we have been delighted to 
see him return again and again to Singapore, and as leader of the Royal Society’s expedi- 
tions of 1961 and 1964 to Kinabalu in Sabah and of 1965 to the Solomon Islands. 


This note started as a brief introduction to the articles that follow. Write something 
about Corner’s Singapore days, said the Editors of this Festschrift. There is much, but 
let this suffice. 


Salam masera! Lanjutkan usia! 


(All hail! Long Life!) 


Thus we hope it will be with him and with his charming wife, Helga. 


. 7 


— 


E. J. H. Corner’s Botany 
by 


D. J. MABBERLEY 


Botany School, Oxford 


The spirit of our little book is one of progress; although nodding to the past. 
we are looking ahead. Here then, is not the place to list the events of Professor 
Corner’s life, his appointments, wanderings and honours: it has been done before*. 
What has not been written is that courses of Tropical Botany at Cambridge begun 
by Professor Corner and now, alas, discontinued, were an inspiration to generations 
of undergraduates and research students. Further, those beginning in less favourable 
surroundings and hearing Professor Corner as a visiting lecturer, have been led to 
see through the blinkers of that botany which is orientated to the plants of the 
temperate zone and peddled by the pusillanimous, These are the blinkers which 
have dragged the study of the whole plant down to the popular image of “‘pressing 
flowers’, and driven many to the narrow reaches of the esoteric in pursuit of 
academic respectability. Of those fortunate to have been able to shake off such 
tyranny, and of the few who were able to do so at the Botany School in Cambridge 
under Professor Corner’s supervision, J am privileged to say that I was one, 
though the last. 


How did it begin? A new schoolmaster fresk from Cambridge went to Rugby: 
in the sixth form was John Corner. The schoolmaster had read the writings of 
A. H. Church, a remarkable philosopher of botany, then working in the Botany 
School at Oxford. Corner read Church’s unassuming, unillustrated and rather slim 
Oxford Botanical Memoir entitled Thalassiophyta. Despite the tightly argued and 
rather heavy prose, much of which was not understandable to a schoolboy, the 
blinkers fell away. Much of the botany taught at Cambridge, whither he went from 
Rugby, was, in consequence, dull and uninteresting. He cut lectures. He read. In 
1928 he presented a paper (still preserved at the Botany School) on Thalassio- 
phyta to the Botany Club. A friend introduced him to Church, and, whilst still a 
research student in mycology at Cambridge, he travelled to Oxford to see Church 
and became his disciple. Church’s works and teaching, unfashionable at the time, 
reflected an astounding vision and an unparalleled grasp of the fundamental 
problems of botany. He, who had never ventured beyond Plymouth, could 
discourse on the floras of the world. When Corner set out for the forests of 
Malaya, Church advised him, “‘Note everything! Draw everything! Photograph 
everything!”’, advice passed through Corner to his pupils, and now to Church’s 
“great-grand-pupils”’. 

This is not the only legacy as we hope this volume shows. It reflects Professor 
Corner’s interests as shown by comparison with his list of publications. Some of 
the papers are controversial: Professor Corner’s writings have never avoided 
controversy. Obvious are the Durian Theory, the new classification of Clavaria, 
as well as papers on conservation and the teaching of botany which have encouraged 
and excited discussion. 


* Flora Malesiana I, 1: 117-118 (1950) & I, 8: XXVI (1974); Biol J. Linn. Soc, 2: 322-324 
(1970); Who’s Who: 680 (1975); Flora Malesiana Bull. (29): 2536-2538 (1976). 


4 Gardens’ Bulletin, Singapore — X XIX (1977) 


The Indomalayan flora and ‘“‘funguses”, figs and breadfruit, durians and 
pachycauls; from trees, their form and evolution, to trees and man, to trees in 
horticulture and trees in conservation — a few of his subjects. And so here is 
offered Stearn’s paper on the impact of tropical rain forest on those introduced 
to it for the first time; Ashton on the ecology of the Durian Theory; Soepadmo 
and Eow on the reproductive biology of Durio itself; Jarrett on the construction of 
the syncarp of Artocarpus; Mabberley on the afroalpine pachycaul flora; White on 
the origins of African geoxylic suffrutices, the final bars of the leptocaul opera; 
remarks on the evolution of rainforest herbs by Burtt. Brunig & Klinge compare 
the structure of forests in Borneo and South America. Van Steenis takes up the 
question of differing modes of evolution in animals and plants, while Fedorov 
deals with the ‘Vavilovian’ evolution he sees in Dipterocarpaceae. Stone sets down 
the infrageneric classification of Pandanus, pachycaul monocotyledons par 
excellence, Of the Malayan flora so well known to Professor Corner, Hsuan Keng 
describes a new species of Theaceae and Holttum monographs a group of 
thelypterid ferns, whilst David and Jaquenoud describe new Tremellales from 
Singapore. Perreau & Heim continue the mycological papers with a new Boletus 
whilst developmental anatomy is represented by Fahn & Joel’s paper on the 
secretory ducts of the mango, and Sporne presents an essay on the enigmatic 
girdling bundles of dicotyledonous flowers. The construction studies pioneered by 
Professor Corner are represented by the paper of Hallé and Mabberley on primitive 
tree-forms while the origin of primitive flowering plants is tackled from a different 
angle by Thorne. Professor Corner’s monographic work on Asian and Australian 
Ficus is here complemented by a study of the origin of the sycomore in the Middle 
East by Galil and co-workers, and by Wiebes’s history of fig wasp research. The 
importance and limits of taxonomy are stressed by Heywood and the problems 
and objectives of Flora-writing by Frodin, whilst Menninger ends the volume with 
a consideration of the aesthetic importance of trees in tropical and subtropical 
horticulture. 


Although Professor Corner has retired, the flow of work is unabated. The 
monumental Seeds of Dicotyledons which appeared in 1976, is the fruit of over 
thirty years’ painstaking investigation and interpretation, whilst even now in Shelford 
surrounded by his books, notes and collections in a veritable thesaurus botanicus, 
enlarged to contain his fungus herbarium and other specimens, he is writing up the 
flora of the Sedili River in eastern Johore! 


List of Publications 
(excluding reviews, letters and reports of discussion) 


(To 1 January 1977)* 


CORNER, E. J. H. (1927). A cytological investigation of a sport in a plant of 
the garden stock. Proc. Linn. Soc. Lond. 139: 75-77. 


—_—_——— (1929). A Humariaceous fungus parasitic on a liverwort. Ann. Bot. 
43: 491-505. 


(1929). Studies in the morphology of Discomycetes I. The marginal 
growth of apothecia. Trans. Br. mycol. Soc. 14: 263-275. 


(1929). Studies in the morphology of Discomycetes II. The structure 
and development of the ascocarp. Trans. Br. mycol. Soc. 14: 275-291. 


(1930). Studies in the morphology of the Discomycetes III, The 
Clavuleae. Trans. Br. mycol. Soc. 15: 107-120. 


* The compiler is indebted to Mrs. Heap of the Botany School Library, Cambridge for 
assistance, particularly in tracing some of the rarer items. 


E. J. H. Corner’s Botany 5 
(1930). Studies in the morphology of the Discomycetes IV. The 
evolution of the ascocarp. Trans. Br. mycol. Soc. 15: 121-134. 


(1931). Studies in the morphology of the Discomycetes V. The 
evolution of the ascocarp (continued). Trans. Br. mycol. Soc. 15: 332-350. 


(1931). The identity of the fungus causing wet rot of rubber trees 
in Malaya. J. Rubb. Res. Inst. Malaya 3: 120-123. 


(1932). The fruit body of Polystictus xanthopus Fr. Ann. Bot. 
46: 72-111. 


(1932). A Fomes with two systems of hyphae. Trans. Br. mycol. 
Soc. 17: 51-81. 


(1932). The identity of the brown-root fungus. Gdns’ Bull. Straits 
Settl. 5: 317-352. 


(1933). A revision of the Malayan species of Ficus: Covellia and 
Neomor phe. J. Malay. Brch R. Asiat. Soc. 11: 1-65. 


(1934). An evolutionary study in Agarics: Collybia apalosarca and 
the veils. Trans. Br. mycol. Soc. 19: 39-88. 


(1935). The fungi of Wicken Fen, Cambridgeshire. Trans. Br. mycol. 
Soc. 19: 280-287. 


(1935). Observations on resistance to powdery mildews. New 
Phytol. 34: 180-200. 


(1935). A Nectria parasitic on a liverwort: with further notes on 
Neotiella crozalsiana. Gdns’ Bull. Straits Settl. 8: 135-144. 


(1935). Cassia in Malaya. Malay. Agri-hort. Ass. Mag. 5: 37. 


(1935). The seasonal fruiting of agarics in Malaya. Gdns’ Bull. 
Straits Settl. 9: 79-88. 


(1936). Hygrophorus with dimorphous basidiospores. Trans. Br. 
mycol. Soc. 20: 157-184. 


(1938). Annual Report of the Director of Gardens for the year 1937. 
Singapore: Govt, Printing Office. 
(1938). The systematic value of the colour of withering leaves. 
Chronica bot. 4: 119-121. 


(1939). Notes on the systematy and distribution of Malayan 
phanerogams. Part I. Gdns’ Bull. Straits Settl. 10: 1—SS. 


(1939). Notes on the systematy and distribution of Malayan 
phanerogams. Part II. Gdns’ Bull. Straits Settl. 10: 56-81. 


(1939). A revision of Ficus, subgenus Synoecia. Gdns’ Bull. Straits 
Settl. 10: 82-161. 


(1939). Notes on the systematy and distribution of Malayan 
phanerogams. Part III. Gdns’ Bull. Straits Settl. 10: 239-329. 


———————— (1940). Botanical monkeys. Malay Agri-hort. Ass. Mag. 10: 
147-149. 


(1940). Wayside Trees of Malaya, Vol. 1: 770 pp; vol. II: 228 pl. 
Singapore: Government Printing Office [2nd Ed. 1952]. 


168: 1031. 


Gardens’ Bulletin, Singapore — X XIX (1977) 
(1940). Note: larger fungi in the tropics. Trans. Br. mycol. Soc. 
24: 357. 


(1941). The flora of Singapore. Malay. Agri-hort. Ass. Mag. 11: 
59-62. | 


(1941). Further notes on the Moreton Bay Chestnut, (Castano- 
spermum australe). Malay. Agri-hort. Ass. Mag. 11: 151-154. 


(1941). A naturalist’s companion. Malay. Nat. J. 2: 11-14. 


(1941). Notes on the systematy and distribution of Malayan 
phanerogams IV — Ixora. Gdns’ Bull. Straits Settl. 11: 177-235. 


(1946). Suggestions for botanical progress. New Phytol.45: 185-192. 


(1946). Tropical biology — an international problem. Biol. & 
Human Affairs. 12: 53-57. 


(1946). Centrifugal stamens. J. Arnold Arbor, 27: 423-437. 


(1946). The pig-tailed monkey as a plant-collector. Zoo Life 
1: 89-92. 


(1946). Need for the development of tropical ecological stations. 
Nature 157: 377. 


(1947). Variation in the size and shape of spores, basidia and 
cystidia in Basidiomycetes. New Phytol. 46: 195-228. 


(1948). Asterodon, a clue to the morphology of fungus fruit-bodies: 
with notes on Asterostroma and Asterostromella. Trans. Br. mycol. Soc. 31: 
234-245. 


(1948). Studies in the basidium 1, The ampoule effect, with a note 
on nomenclature. New Phytol. 47: 22-49. 


(1949). The Annonaceous seed and its four integuments, New 
Phytol. 48: 332-364. 


(1949). The Durian Theory or the origin of the modern tree. Ann. 
Bot. (N.S.) 13: 367-414: translated (1964) as ‘‘La théorie du Durian ou 
Porigine de lVarbre modern. Adaptation francaise par N. & F. Hallé” 
Adansonia (N.S.) 4: 156-184. 


(1950). A Monograph of Clavaria and allied Genera, Ann. Bot. 
Mem. 1: 740 pp. + 16 pl. 


(1950). Descriptions of two luminous tropical agarics (Dictyopanus 
and Mycena). Mycologia 42: 423-431. 


(1950). Report on fungus-brackets from Star Carr, Seamer. Pp. 
123-124 in F. G. D. Clark, Preliminary report on excavations at Star Carr, 
Seamer, Yorkshire (Second season 1950). Proc. prehist. Soc. 1950 (9): 109-129. 


(1951). Prof. H. Tanakadate, Nature 167: 586. 
— (1951). The Leguminous seed. Phytomorphology 1: 117-150. 
(1951). Lectotypes in mycology: a taxonomic proposal. Nature 


(1952). Durians and dogma, /ndones. J. nat. Sci. 5-6: 141-145. 


—— (1952) Generic names in Clavariaceae. Trans. Br. mycol, Soc. 
35: 285-298. 


E. J. H. Corner’s Botany 7 


(1952). Addenda Clavariacea I. Two new Pteruloid genera and 
Deflexula. Ann. Bot. (N.S.) 16: 269-291. 


(1952). Addenda Clavariacea II. Pterula and Pterulicium. Ann. Bot. 
(N.S.) 16: 531-569. 


(1953). Addenda Clavariacea III. Ann, Bot. (N.S.) 17: 347-369. 


(1953). The construction of polypores — I. Introduction: Polyporus 
sulphureus, P. squamosus, P. betulinus and Polystictus microcylus. Phytomor- 
phology 3: 152-167. 


(1953). The Durian Theory extended — I. Phytomorphology 3: 
465-476. 


(1953). Proposal No. 10, principles for stability of nomenclature 
(VIIIth Int. Bot. Congr. prop. 10). Taxon 2: 101. 


& L. E. HAWKER (1953). Hypogeous fungi from Malaya. Trans. 
Br. mycol. Soc. 36: 125-137. 


(1954). The classification of higher fungi. Proc. Linn. Soc. Lond. 
165: 4-6. 

(1954). The Durian Theory extended — II. The arillate fruit and 
the compound leaf. Phytomorphology 4: 152-165. 


(1954). The Durian Theory extended — III. Pachycauly and 
megaspermy — Conclusion. Phytomorphology 4: 263-274. 


(1954). Evolution of tropical rainforest. Pp. 34-46 in J. Huxley, 
A. C. Hardy & E. B. Ford (eds.), Evolution as a Process. London: Allen & 
Unwin. 


(1954). Further descriptions of luminous agarics. Trans. Br. mycol. 
Soc. 37: 256-271. 


(1955). Botanical coilecting with monkeys. Proc. R. Instn Gt Br. 
36 (no. 162): 1-16. 


———_—— (1955). Epilogia [sic] pro monographia sua. Taxon 4: 6-8. 


(1956). Taxonomy and tropical plants. Proc. Linn. Soc. Lond. 
168: 65-70. 


(1956). A new European Clavaria: Clavulinopsis septentrionalis 
sp. nov. Friesia 5: 218-220 


K. S. THIND & G. P. S. ANAND (1956). The Clavariaceae of the 
Mussoorie Hills (India) II. Trans. Br. mycol. Soc. 39: 475-484. 


(1957). Craterellus Pers., Cantherellus Fr. and Pseudocraterellus 
gen. nov. Sydowia, beih. 1, Festschr. f. Franz Petrak: 266-276. 


(1957). Some Clavarias from Argentina. Darwiniana 11: 193-206. 


» K. S. THIND & SUKH DEV (1957). The Clavariaceae of the 
Mussoorie Hills (India) VII. Trans. Br. mycol. Soc. 40: 472-476. 


-—————. (1958). The Clavariaceae of the Mussoorie Hills (India) IX. Trans 
Br. mycol. Soc. 41: 203-206. 


(1958) Transference of function. J. Linn. Soc. Bot, 90: 33-40: J. 
Linn. Soc. Zool. 44: 33-40 


8 Gardens’ Bulletin, Singapore — X XIX (1977) 
(1958). An introduction to the distribution of Ficus. Reinwardtia 
4: 15-45 


CASH, E. K. & E. J. H. CORNER (1958). Malayan and Sumatran Discomycetes. 
Trans. Br. mycol. Soc. 41: 273-282. 


CORNER, E. J. H. (1959). Vegetation of the humid tropics. Nature 183: 795-796. 


——_—_—— (1959). The importance of tropical taxonomy to modern botany. 
Gdns’ Bull. Singapore 17: 209-214. 


(1960). Taxonomic notes on Ficus Linn., Asia and Australasia. 
I-IV. Gdns’ Bull. Singapore 17: 368-485. 


(1960). The Malayan flora. Pp. 21-24 in R. D. Purchon (ed.), Proc. 
Centen. & Bicenten. Cong. Biol., 1958 (Singapore). 


(1960). Taxonomic notes on Ficus Linn., Asia and Australasia. 
V-VI. Gdns’ Bull. Singapore 18: 1-69. 


(1961). Impact of man on the vegetation of the humid tropics. 
Nature 189: 24-25. 


(1961). Agnes Arber. Phytomorphology 11: 197-198. 


(1961). A tropical botanist’s introduction to Borneo. Sarawak 
Mus. J. 10: 1-16. 


(1961). Taxonomic notes on Ficus Linn., Asia and Australasia. 
Addendum. Gdns’ Bull. Singapore 18: 83-97. 


(1961). Introduction. Pp 1-7 in J. Wyatt-Smith & P. R. Wycherley 
(eds), Nature Conservation in Western Malaysia, Kuala Lumpur: Malay. 
Nat. Soc. 


(1961). Evolution. Pp. 95-115 in A. M. McLeod & L. S. Cobley 
(eds), Contemporary Botanical Thought. Edinburgh: Oliver & Boyd. 


(1961). A note on Wiesnerina (Cyphellaceae). Trans. Br. mycol. 
Soc. 44: 230-232. 


CORNER, E. J. H. & K. S. THIND (1961). Dimitic species of Ramaria (Clava- 
riaceae). Trans. Br. mycol. Soc. 44: 233-238. 


(1962). Botany and prehistory. Pp. 38-41 in [U.N.E.S.C.0.], 
Symposium on the Impact of Man on the Humid Tropics Vegetation, Goroka 
1960. 


(1962). The Royal Society Expedition to North Borneo, 1961. 
Emp. For. Rev. 1962: 224-233. 


(1962). The classification of Moraceae. Gdns’ Bull. Singapore 
19: 187-252. 


(1962). Taxonomic notes on Ficus L., Asia and Australasia. 
Addendum II. Gdns’ Bull. Singapore 19: 385-415. 


& C. BAS (1962). The genus Amanita in Singapore and Malaya. 
Persoonia 2: 241-304. 


(1963). The tropical botanist. Advmt Sci, Lond. 20: 328-334. 


(1963). Ficus in the Pacific region. Pp. 233-249 in J. L. Gressitt 
(ed), Pacific Basin Biogeography. Honolulu: Bishop Mus. Press. 


E. J. H. Corner’s Botany 9 
(1963). A criticism of the gonophyll theory of the flower. 
Phytomorphology 13: 290-292. 


(1963). A Dipterocarp clue to the biochemistry of Durianology. 
Ann. Bot. (N.S.) 27: 339-341. 


(1963). Studies in the flora of Thailand 16. Moraceae. Dansk Bot. 
Ark. 23: 19-32. 


(1936). Exploring North Borneo. New Scient. 366: 488-490. 


(1963). Royal Society Expedition to North Borneo 1961: reports. 
Proc. Linn. Soc. Lond. 175: 9-32 (General Report); 37-45 (Special Reports). 


(1964). The Life of Plants. Pp. 315 + 41 pl. London: Weidenfeld 
& Nicholson. [Also trans. Léo Dilé as La Vie des Plantes (1964), and trans. 
Lucia Maldacea as La Vita delle Plante (1972), both with additional pp. 
after p. 316 by P. Coursin.] 


(1964). A discussion of the results of the Royal Society Expedi- 
tion to North Borneo, 1961. Organized by E. J. H. Corner. Proc. R. Soc. Lond. 
B161: 1-91 (Commentary on the general results: pp. 3-6; Conclusion: pp. 
90-91). 


(1965). Check-list of Ficus in Asia and Australasia with keys to 
identification. Gdns’ Bull. Singapore 21: 1-186. 


(1965). Mount Kinabalu East. Sabah Soc. J. No. 4: 170-187. 


(1966). A Monograph of Cantharelloid Fungi. Ann. Bot. Mem. 
2: 255 pp. + 5 pl. 


(1966). The Natural History of Palms. Pp. 393 + 24 pl. London: 
Weidenfeld & Nicholson. 


(1966). Debunking the New Morphology. New Phytol.65: 398-404. 


(1966). Species of Ramaria (Clavariaceae) without clamps. Trans. 
Br. mycol. Soc. 49: 101-113. 


(1966). Kinabalu. Straits Times Annual 1966: 34-37. 
(1966). On Clavaria inaequalis Fr. Nova Hedwigia 12: 61-63. 


(1966). The clavarioid complex of Aphelaria and Tremelloder- 
dropsis. Trans. Br. mycol. Soc. 49: 205-211. 


(1966). Paraphelaria, a new genus of Auriculariaceae. Persoonia 
4: 345-350. 


(1967). Ficus in the Solomon Islands and its bearing on the post- 
Jurassic history of Melanesia. Phil. Trans. R. Soc. Lond. B253: 23-159. 


(1967). On thinking big. Phytomorphology 17: 24-28. 
——————— (1967). Notes on Clavaria. Trans. Br. mycol. Soc. 50: 33-44. 


(1967). Clavarioid fungi of the Solomon Islands. Proc. Linn. Soc. 
Lond. 178: 91-106 


(1967). Biological expeditions. May & Baker Lab. Bull. 7: 90-92. 


(1967). Moraceae. [Bot. Rep. Danish Noona Dan Expedition]. 
Dansk bot. Ark. 25: 64-67. 


10 Gardens’ Bulletin, Singapore — X X1X (1977) 


(1968). A monograph of Thelephora (Basidiomycetes). Beih. zur 
Nova Hedwigia 27: 110 pp + 4 pl. 


(1968). Mycology in the tropics— apologia pro monographia sua 
secunda. New Phytol. 67: 219-228. 


(1968). Conservation — future prospects. Biol. Conserv. 1: 21-26. 
(1969). Notes on Cantharelloid fungi. Nova Hedwigia 18: 738-818. 


(1969). A discussion of the results of the Royal Society Expedition 
to the British Solomon Islands Protectorate, 1965. Organized by E. J. H. 
Corner. Phil. Trans R. Soc. Lond. B255: 185-631 (Introduction: 187-188; 
Ficus: 567-570; The botany of Jaagi Is., Santa Isabel: 571-573; Mountain 
‘flora of Popomanusen, Guadalcanal: 575-577; Larger fungi of the Solomon 
Islands: 579; Summary of the discussion: 621-623). 


(1969). The complex of Ficus deltoidea; a recent invasion of the 
Sunda Shelf. Phil. Trans. R. Soc. B256: 281-317. 


(1969). Ficus sect. Adenosperma, Phil. Trans. R. Soc. B256: 
318-355. 


(1969). The conservation of scenery and wild life. Proc. Ceylon 
Asst. Advmt Sci. 2: 220-231. 


(1969). Ecology and natural history in the tropics. Proc. Ceylon 
Asst. Advmt Sci. 2: 261-273. 


WATANABE, K. & E. J. H. CORNER (1969). Illustrated Guide to Tropical 
Plants. 1147 pp. Tokyo: Hirokawa. 


CORNER, E. J. H. (1970). Ficus subgen. Ficus. Two rare and primitive pachycaul 
spscies. Phil.’ Trans, “Ise B259: 353-381. 


(1970). Ficus subgen. Pharmosycea with reference to the species of 
New Caledonia. Phil. Trans. R. Soc. Lond. B259: 383-433. 


(1970). New species of Streblus and Ficus (Moraceae). Blumea 
18: 393-411. 


(1970). Phylloporus Quél. and Paxillus Fr. in Malaya and Borneo. 
Nova Hedwigia 20: 793-822. 


(1970). Supplement to “‘A Monograph of Clavaria and _ allied 
genera’’. Beih. zur Nova Hedwigia 33: 299 pp. + 4 pl. 


(1970). 37. Ficus (Moraceae). Ident. Lists Malaysian Spec.: 
537-648b. Foundation Flora Malesiana. 


(1971). Merulioid fungi in Malaysia. Gdns’ Bull. Singapore 25: 
355-381. 


(1971). Mycological reports from New Guinea and the Solomon 
Islands. 4, Enumeration of the Clavariaceae, Bull. natn Sci. Mus., Tokyo 
$4: 423-427. 


(1972). New taxa of Ficus (Moraceae). Blumea 20: 427-432. 


(1972). Studies in the basidium — spore space and the Boletus 
snore. Gdns’ Bull. Singapore 26: 159-194. 


(1972). Boletus in Malaysia. 263 pp. +- 23 p. Singapore: Govt. 
Printing Office. 


E. J. H. Corner’s Botany 1] 


(1972). 43. Ficus (Moraceae) from India, Burma, Thailand, China, 
Korea, Japan, Ryu Kyu, Formosa and Hainan, Ident. Lists Malaysian Spec.: 
735-784. Foundation Flora Malesiana. 


(1972). Urgent exploration needs: Pacific Floras. Pac. Sci. Assoc. 
Inform. Bull. 24: 17-27. 


(1974). Boletus and Phylloporus in Malaysia: further notes and 
descriptions. Gdns’ Bull. Singapore 27: 1-16. 


(1975). New taxa of Ficus (Moraceae) 2. Blumea 22: 299-309. 


(1975). Prototypic organisms XIII. Tropical trees. Theoria to 
Theory 9: 33-43. 


(1975). The evolution of Streblus Lour. (Moraceae): with a new 
species of sect. Bleekrodea. Phytomorphology 25: 1-12. 


(1975). Ficus in the New Hebrides. Phil. Trans. R. Soc. Lond. 
B 272: 343-367. 


(1976). The climbing species of Ficus: derivation and evolution. 
Phil. Trans. R. Soc. Lond. B 273: 379-386. 


(1976). The Seeds of Dicotyledons. Vol. I: 311 pp.; Vol. II: 
552 pp. Cambridge: Cambridge University Press. 


—— (1976). Further notes on Cantharelloid fungi and Telephora. Nova 
Hedwigia 27: 325-342. 


—_———_ (1976). A new species of Parartocarpus Baillon (Moraceae). 
Gdns’ Bull, Singapore 28: 183-190. 


(in press). The freshwater swamp-forest of south Johore and 
Singapore. Gdns’ Bull. Singapore, Supp. 1. 


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The Earliest European Acquaintance 
with Tropical Vegetation 


by 
WILLIAM T. STEARN 


British Museum (Natural History), London 


“Das Glanzstiick der botanischen Mitteilungen tiber ost-indische Pflanzenwelt 
die unter Alexander erschienen, ist die Schilderung des riesigen Feigenbaums, des 
Banyan,” wrote Hugo Bretzl in his massive work on the botanical results of 
Alexander the Great’s invasion of northern India in 326-325 B.C., Botanische 
Forschungen des Alexanderzuges (1903). With this account of the banyan (Ficus 
benghalensis L.) preserved in Theophrastus’s Enquiry into Plants ( péri phuton 
historia), there began well over two thousand years ago the European investiga- 
tion of the genus Ficus in tropical Asia to which Professor John Corner has made 
such illuminating contributions. Theophrastus (370-c.285 B.C.) himself never went 
to India; as a pupil first under Plato, then under Aristotle, whose library and 
garden he inherited, and later as an academic teacher, he spent almost all his life 
in Athens. His career spanned completely the life of Alexander (356-323 B.C.), 
whose army undoubtedly included well-educated highly intelligent observers and 
recorders, and the reports of these officers came into Theophrastus’s hands, Their 
firsthand accounts disappeared long ago but parts have survived, being embedded, 
like fragments of Roman masonry in medieval walls, within the writings of others, 
notably Theophrastus and Arrian, and among them is the description of the banyan, 
the Indian fig (suké hé indiké), praised so highly by Bretzl. This occurs in 
Theophratus’s Enquiry IV. iv. 4-S. 


Since so much of Professor Corner’s life, research and writing has been 
devoted to the study of tropical plants, particularly those of Indo-Malaya, the 
celebration of his seventieth birthday provides a fitting occasion on which to bring 
to notice again these first records of the impact of tropical vegetation upon the 
receptive analytic Western mind. 


Even for a present-day young botanist versed firsthand only in the north 
temperate flora, first acquaintance with the strange diverse vegetation of the tropics, 
with plants of a luxuriance and character unknown in Europe and North America, 
is a stimulating and mentally bewildering or overwhelming experience. A succession 
of narratives indicate that this has always been so. 


Thus Henry Walter Bates arrived with Alfred Russel Wallace at Para, Brazil, 
on 28 May 1848, having left Liverpool on 26 April. They immediately walked 
across the town, then small and closely encompassed by native vegetation. ““The 
impressions received during this first walk,’ Bates wrote in his The Naturalist on 
the River Amazons (1863) after eleven years in the Amazon valley, “can never 


wholly fade from my mind ... ... so striking, in the view, was the mixture of 
natural riches and human poverty ... ... But amidst all, and compensating every 
defect, rose the overpowering beauty of the vegetation ... ... Strange forms of 


vegetation drew our attention at every step.” Tropical fruit trees, tall palms with 
smooth columnar stems, epiphytes perched amid boughs, slender woody lianes, 
luxuriant creeping plants overrunning alike tree-trunks, roofs and walls, sword- 
leaved bromeliads and many other plants remarkable in leaf, stem or manner of 


13 


14 Gardens’ Bulletin, Singapore — X XIX (1977) 


growth together exemplified for them “‘the teeming profusion of Nature’, to which, 
as night came on, the whirring of cicadas, the shrill stridulation of grasshoppers, 
each sounding its peculiar note, the hooting of tree frogs, the croaking of toads 
and frogs in pools together provided an audible expression almost deafening. This 
rich diversity had earlier affected Alexander von Humboldt and Aimé Bonpland 
as vividly. They arrived at Cumana, Venezuela, on 16 July 1799, having sailed 
from Spain on 4 June 1799. The effect of the tropical environment upon both the 
travellers led Alexander to write to his brother Wilhelm: ‘What trees! Coco-nut 
trees 50-60 feet high; Poinciana pulcherrima* with a foot high bouquet of magni- 
ficent bright red flowers; pisang and a host of trees with enormous leaves and 
scented flowers, as big as the palm of a hand, of which we knew nothing ... ... We 
rush around like the demented; in the first three days we were unable to classify 
anything; we pick up one object to throw it away for the next. Bonpland keeps 
telling me he will go mad if the wonders do not cease.” 


Even earlier James Wallace (d. 1724), an Orkney man who had taken part 
in the ill-fated Scottish attempt of 1698-1700 to found a colony at Darien, Panama, 
wrote: ““This place affords legions of monstrous plants enough to confound all the 
methods of Botany ever hitherto thought upon ... ... some of their leaves exceed 
three ells in length and are very broad, besides these Monsters, reduceable to no 
Tribe, there are here a great many of the European kindred but still something 
odd about them’’. The equally remarkable tropical vegetation of Amboina in the 
East Indies inspired Georg Everard Rumpf. (c. 1627-1702) to the vast task of 
preparing his Herbarium Amboinense (6 vols, 1741-1750) which describes vividly 
and accurately some 1200 species. 


In southern India the governor of the Dutch possessions along the Malabar 
coast, Hendrik Adriaan von Rheede tot Draakenstein (1637-1692), was so 
impressed by the diversity of plants there, particularly by the epiphytes — ‘“‘on 
one tree ten or twelve different sorts of leaves, flowers and fruits might be met 
with,”’ as he said — that he set in hand the preparation of a detailed account, on 
which were engaged himself, an Italian missionary, about sixteen learned Brahmins, 
four artists and various native collectors. His Hortus Indicus Malabaricus (12 
vols. folio, 1678-1703) was the first major work to bring a tropical flora to the 
notice of stay-at-home botanists in Europe. He introduced the banyan into cultiva- 
tion at Amsterdam. 


These works were by-products of European conquest and dominion, above 
all of the establishment of the Dutch empire in the East Indies during the 18th 
century A.D., an empire reached only after a long and hazardous voyage around 
Africa. The first European contact with tropical vegetation likewise resulted from 
European empire-building in Asia, but was made overland in the 4th century B.C. 
Having defeated Darius in 331, Alexander marched his army into Turkistan 
(Bactria) and then in 327 invaded north-western India by way of the Khyber Pass 
and entered the Punjab; the river Indus became the eastern boundary of his 
extended Asiatic empire. Short-lived though this was, it led to a flow of Greek 
ideas and art into northern India and a flow of information about the country 
back to Greece. Such information must have been very extensive, since the 
surviving fragments of it, preserved in the writings of Theophrastus, Plutarch, 
Strabo and Pliny, for example, embrace Indian customs and geography as well as 
plants. Bretzl has so exhaustively collected all which is available of a botanical 
nature that were his book better known and easy to acquire — it seems to be 
scarce, is accessible in few libraries and has never been translated — there would 
be little justification for calling attention to this here. It deserves, however, not to 
be forgotten. 


* Caesalpinia pulcherrima (L.) Swartz. 


Tropical vegetation, European acquaintance 15 


The banyan (Ficus benghalensis L.) is an evergreen tree widespread in India 
with entire leathery leaves and small red fruits, and rises to about 26 m. (85 feet) and 
by pushing down, from its horizontally spreading branches, supporting prop- or 
pillar-roots at intervals, spreads over so wide an area that, as Corner has said, it 
“develops the biggest crown of any plant in the world’’, One individual tree can 
thus make a small wood. 


This habit of the banyan, sending down aerial roots from its 
branches away from the main stem, caught Greek attention. It raised moreover 
an interesting morphological question such as indeed could only be seen as a 
question when the study of plants had passed from being purely utilitarian, as was 
presumably that of unlettered herb-gatherers, the rhizotomoi (literally ‘root-cutters’), 
to being scientific and philosophical as was that of Theophrastus and his associates, 
namely the distinction between root and shoot. Clearly Theophrastus rejected the 
common view that any underground organ of a plant is a root, in other words, that 
all underground parts are homologous, by emphasizing the differences between the 
tuber of arum, the bulbs of squill, garlic and onion and the roots they send out. 
“His whole treatment of the subject of the roots of plants reads as if he had gone 
stealthily to work,” so E. L. Greene wrote in 1909, “‘to undermine an old and 
everywhere received opinion that roots are simply the underground parts of plants.” 
He based his definition on natural function and not position. This means that roots 
like shoots can be aerial and the banyan, though he can never have seen it himself, 
had been so well described, possibly even sketched, by Greek observers in India 
that it provided a most remarkable example of them. ‘“‘The character and function 
of the roots of the Indian fig are peculiar, for this plant sends out roots from the 
shoots until it has a hold upon the ground and roots again; and so there comes 
to be a continuous circle of roots around the tree, not connected with the main 
stem but at a distance from it” (Loeb Classical Library translation by A. Hort, 
1: 41; 1916). 


Theophrastus had indeed made a detailed study, very remarkable for his 
period, of the underground parts of plants, distinguishing between rhizomes, tubers, 
bulbs and roots and distinguishing within the last-named various types, a matter 
discussed by Greene (1909), Str6mberg (1937) and Arber (1950). 


Theophrastus’s fuller account of the banyan occurs later in his work, in a 
section on trees and herbs special to Asia: “The Indian land has its so-called 
fig-tree which drops its roots from its branches every year, as has been said above, 
and it drops them not from the new branches, but from those of last year or even 
from older ones; these take hold of the earth and make, as it were a fence about 
the tree, so that it becomes like a tent, in which men sometimes even live. The 
roots as easily distinguished from the branches being whiter, hairy, crooked and 
leafless, The foliage above is also abundant and the whole tree round and 
exceedingly large. They say that it extends its shade for as much as two furlongs; 
and the thickness of the stem is in some instances more than sixty paces, while 
many specimens are as much as forty paces through. The leaf is quite as large as a 
shield, but the fruit is very small, only as large as a chick-pea, and it resembles a 
fig. And that is why the Greeks named this tree a ‘fig-tree’. The fruit is curiously 
scanty, not only relatively to the size of the tree, but absolutely. The tree also 
grows near the river Akesines’’. The mixture here of plain fact and of exaggeration 
Suggests strongly that it is a description made from memory, perhaps told to 
Theophrastus by a soldier returned from India. Thus the leaves of the banyan, 
though up to 20 cm. long and, 12 cm. broad, are much smaller than the smallest 
round shield (pelté, Latin pelta) of the Ancient Greeks. Nevertheless, in addition 
to the general description of habit, this account contains two very significant 
remarks. The tree’s prop-roots, though aerial, woody and stem-like, are distin- 
guished from stems by being leafless (aphulloi seems a more correct rendering than 
the diphulldi of most codices). Moreover the fruits are compared to those of the 


16 Gardens’ Bulletin, Singapore — XX1X (1976) 


fig (suké, Ficus carica L.) on account of their structure, though not their size; 
hence the Greeks classified the banyan as a fig, swké hé indiké; this indicates real 
taxonomic insight since the banyan, except for these, is so utterly different from 
the cultivated Mediterranean figs. 


Theophrastus also mentions in Book IV. iv. 5 other Indian plants, e.g. a very 
large tree with a large sweet fruit, presumed to be the jack-fruit (Artocarpus 
heterophyllus Lam.), another with a crooked sweet fruit, presumed to be the mango, 
(Mangifera indica L.), one with a fruit like the cornelian cherry (Cornus mas 
L.), presumed to be the jujube (Zizyphus jujuba Mill.), and another with an oblong 
leaf, like the feathers of the ostrich, 2 cubits (3 feet) long, presumed to be the 
banana (Musa). 


The clothes of the Greeks were made from linen, hemp and wool. In India 
they found people wearing clothes that were the product of a tree with a leaf like 
the mulberry but resembling the wild rose; this was cotton (Gossypium); the plants 
were grown in the plains in rows, so that seen from a distance they looked like 
vines. 


The mangroves on the sea-coast provided another kind of tropical vegetation 
wholly strange to men from the Mediterranean region, which has no counterparts 
to these trees growing in tidal waters and partly submerged at high tide. In 
December 325 B.C. the Cretan admiral Nearchus with a fleet built for Alexander 
on the Hydaspes (now the Jhelum) river sailed into the Persian Gulf from Pattala 
(now Tatta east of Karachi), then at a mouth of the Indus though now inland, 
while Alexander marched his army into Gedrosia, the modern Makran region of 
Baluchistan and adjacent southern Iran, evidently along the coast over part of the 
way, for Arrian, quoting Aristobulus, records mangrove trees: “‘one, with a leaf 
like laurel, is found growing below high-water mark on the sea-shore; this tree 
is left high and dry by the ebb tide, and on the succeeding flood looks as if it were 
growing in the sea. Some of them, growing in hollows which do not dry at low 
tide, are never out of the water, but even so take no harm from the constant 
immersion of their roots. Some trees are as much as 45 feet in height and were 
in blossom when Alexander saw them; the flower is rather like the white violet 
[i.e. stock, Matthiola incana (L.) R. Br.] but much more fragrant” (Arrian, Life 
of Alexander the Great, transl. A. de Sélincourt, 214; 1958). This was either 
Avicennia marina (Forsk.) Vierh. or Rhizophora mucronata Lam. 


An essentially similar account, derived evidently from Nearchus’s voyage past 
the mangrove-fringed creeks on the northern coast of the Persian Gulf, occurs in 
Theophrastus’s Enquiry, IV. vii: ““There are plants in the sea which they call 
‘bay’ [daphné, Laurus nobilis L.] and olive [élaia, Olea europaea L.] In foliage 
the ‘bay’ is like the aria [aria, holm oak, Quercus ilex L.], the ‘olive’ like the real 
Olive. The latter has a fruit like olives.”” To this Theophrastus added: “‘On the 
islands which get covered by the tide they say that great trees grow, as big as 
planes or the tallest poplars, and that it came to pass, that when the tide came up, 
while the other things were entirely buried, the branches of the biggest trees 
projected and they fastened the stern cables to them, and then, when the tide 
ebbed again, fastened them to the roots. And that the tree has a leaf like that of 
the bay, and a flower like gilli-flowers [i6n, Matthiola incana] in colour and smell, 
and a fruit the size of that of the olive, which is also very fragrant. And it does 
not shed its leaves, and that the flower and the fruit form together in autumn and 
are shed in spring.” The roots to which the ships were fastened at low tide must 
have the prop-roots of Rhizophora, but evidently the Greeks were not there at the 
right time to observe the viviparous germination of the fruit; otherwise they would 
surely have noted the long club-shaped radicle produced while the fruit still clings 
to the bough. 


Theophrastus also incorporated observations referring to Avicennia marina 
made on the northern coast of the Persian Gulf, probably in the Strait of Hormuz 


Tropical vegetation, European acquaintance 17 


near Bandar-Abbas, southern Iran: “In Persia in the Carmanian district where 
the tide is felt there are trees of fair size like the andrachne [andrachlé, Arbutus 
andrachne L.] in shape and leaves; and they bear much fruit like in colour to 
almonds on the outside but the inside is coiled up as though the kernels were all 
united”. This obviously refers to the longitudinally folded cotyledons, one 
enclosing the other, in the seed of Avicennia. ““These trees are all eaten away up 
to the middle by the sea and are held up by their roots”. 


Through an exploratory voyage by Androsthenes along the southern coast 
of the Persian Gulf the Greeks also became acquainted with the island of Tylos, 
a very ancient centre of trade and civilization, now known as Bahrain, and 
recorded some of the plants grown there, as noted by Theophrastus. These included 
cotton, date palms, an evergreen fig and vines. They also stated “‘that there is 
another tree with many leaves [i.e. leaflets] like the rose and that this closes at 
night but opens at sunrise and by noon is completely unfolded; and at evening 
again it closes by degrees and remains shut at night, and the natives say that it goes 
to sleep”. This is the first record of the sleep-movement of the tamarind (Tamar- 
indus indica L.), indeed of any plant. 


Bamboos are so important in the rural economy of India and grow there to 
so much greater heights than those of the two similar plants known to the Greeks, 
the common reed (Phragmites australis (Cav.) Trin. ex Steud.) and the giant reed 
(Arundo donax L.), that it would be strange indeed if the Greeks had failed to 
mention them at all. Theophrastus’s reference to them in his Enquiry IV. xi. 13 
is, however, brief: ‘““The Indian reed is very distinct and as it were of a wholly 
different kind; the ‘male’ is solid and the ‘female’ hollow ... ... a number of reeds 
of this kind grow from one base and they do not form a bush, the leaf is not long, 
but resembles the willow leaf, these reeds are of great size and good substance, so 
that they are used for javelins’. The terms ‘male’ and ‘female’ are used here 
metaphorically as they were for other plants, excluding however the date-palm; 
the ‘male’ has been identified as Dendrocalamus strictus (Roxb.) Nees, the ‘female’ 
as Bambusa arundinacea (Retz.) Willd. 


Since Theophrastus, Arrian and other Ancient Greek writers only incorporated 
such information about tropical plants and vegetation as was relevant to their own 
work, almost indeed incidentally, it is reasonable to believe that the sources whence 
this came must have contained much more which has long been lost. Theophrastus’s 
task in his botanical writings — he also wrote on astronomy, education, ethics, 
logic, mathematics, odours, meteorology, religion and rhetoric — was to bring 
together an immense quantity of information, no small part based upon his own 
observations, which he presented in a classified form, using facts not simply for 
themselves but also to provide examples for general statements, giving particular 
attention to differences which delimited or expressed the essential nature of subjects. 
It was his intention not to list all the known individual kinds of plants but simply 
those characteristic of certain features or regions. His fourth book in the Enquiry 
deals with the plants special to particular districts and habitats; in the sections 
relating to Asia, since he had never been there himself, he accordingly extracted 
what seemed especially interesting or relevant from the writings and recollections 
of his contemporaries who had accompanied Alexander on his invasion of India. 
Indeed he said “‘there are also many more different from these found among the 
Hellenes, but they have no names, There is nothing surprising in the fact that these 
trees have so special a character; indeed, as some say, there is hardly a single tree 
or shrub or herbaceous plant, except a few, like those in Hellas”’. 


The task of Arrian, who lived some four hundred years later, was to write a 
reliable biography of Alexander, again taking what seemed relevant from earlier 
sources. The loss of these sources is not surprising. Thus the immense libraries of 
Pergamon and Alexandria had virtually perished by the 5th Century A.D., their 


18 Gardens’ Bulletin, Singapore — XX1X (1976) 


decline hastened by fanatical Christians who regarded them as pernicious reposito- 
ries of pagan literature. Because of this, the effect upon the Hellenic world of the 
new knowledge stemming from Alexander’s Asiatic conquests can only be dimly 
surmised. In the field of botany it enlarged European vision by bringing to notice 
plant structures, such as the banyan with its prop-roots, and ways of life, such as 
that of the mangroves growing as trees within the sea, as well as individual plants, 
which had no counterparts in Europe. Various European plants perform nyctitropic 
movements of the leaflets but none so conspicuously as does the tamarind. This 
extension of biological concepts through contact with tropical vegetation is 
necessary to counteract the impoverishing narrowness of outlook and experience 
which afflicts botany taught from a few plants in the laboratory by teachers who 
have never felt the excitement of seeing the plant world in its most complex form, 
above all in tropical rain forest regions, As Professor Corner has said in the last 
chapter of his The Life of Plants (1964), “‘high rainfall, sunshine and temperature 
make the tropical forest the prime of plant life ... ... But the forests, which show 
how trees were made, are going. They are vanishing nowhere faster than from the 
alluvial plains where the vestiges of the last creative phase of plant life, that 
prepared the way for the modern world, may survive’’. Because Professor Corner, 
with a stimulating breadth of outlook fostered in the tropical environment of 
Malaya, has striven so much to make stay-at-home European botanists aware of 
the evolutionary significance of tropical plants and the urgent need to study them 
before destruction of their habitats deprives humanity of many of them forever, 
it has been appropriate to recall here the first chapter in the history of European 
botanical contact with their challenging diversity. 


Some Sources of Further Information 


ARBER., A. 1950. The Natural Philosophy of Plant Form, Cambridge University 
Press. 


ARRIAN. 1958. The Life of Alexander the Great, Transl. by A. de Sélincourt. 
London, Penguin Books. 


BRETZL, H. 1903. Botanische Forschungen des Alexanderzuges. Leipzig. 


GREENE, E. L. 1909, Landmarks of Botanical History, Part 1 (Prior to 1562 
A.D.). Washington, D.C. 


SENN, G. 1934. Die Pflanzenkunde des Theophrast von Eresos. Basel. 


STEARN, W. T. 1957. Botanical exploration to the time of Linnaeus, Proc. Linn. 
Soc. Lond. 169 (sess. 1956-57): 173-196. 


STROMBERG, R. 1937. Theophrastea: Studien zur botanischen Begriffsbildung. 
(Géteborgs Kungl. Vet. Handl. V. A. 6 no 4). Goteborg. 


THEOPHRASTUS. 1916. Enquiry into Plants, Transl. by A. Hort. 2 vols. (Loeb 
Classical Library). London & New York. 


Ecology and the Durian Theory 
by 
P. S. ASHTON 


Department of Botany, University of Aberdeen 


The Durian Theory (Corner 1949-1964) is on a base of comparative 
morphology, yet provides insight on the ecology and evolution of tropical forest. 
The hypothetical angiosperm archetype that is deduced from it no longer exists; 
from ecological theory though we may speculate why this is so, and may deduce 
the conditions in which these plants evolved. What ecological bonuses and limita- 
tions does each of the primitive characteristics impose? 


Large spiny loculicidally dehiscent capsule or follicles, with large black seeds more or 
less enveloped in a colourful fleshy aril and dangling on persistent funicles. A large 
seed provides a large food store. essential in the perennial shade of evergreen 
forest. In a windless climate fruit dispersal of forest plants is most effectively 
accomplished by animals, yet the large slowly developing seed must be protected 
from them until ripe. The significance of colour and movement to attract animal 
vectors has been discussed at length by Corner. It is astonishing how disinterested 
even monkeys are with green fruits; we have observed that the embryo and flesh 
of wild rambutan (Xerospermum intermedium Radlk.) fruits matures before the 
pericarp changes from green to yellow, yet the voracious monkeys always failed to 
distinguish maturity before the colour change. Experience of modern trees may have 
led them to fear all green fruits as unpalatable or poisonous; primitive armour, 
once pierced, provides protection against no predator, but the evolution of specific 
poisons reduces attacks to a few specialists. When in Sarawak I had the opportunity 
to identify the food of orangutans set free in Bako National Park, I was struck by 
the dexterity with which they dismembered the horrid defenses of rotan and nibong 
cabbages, and wondered whether these primates might be recent immigrants, 
possibly to the extending Holocene forests; otherwise such plants as the hapaxanthic 
Plectocomia, a particular favourite, would have disappeared as, we can assume, 
already have many other spiny but palatable organisms of former days. 


Moreover, these great spiny primitive fruits are expensive and can only be 
produced in small numbers at a time; they confine those plants that bear them to 
stable habitats where their populations are least likely to suffer large fluctuations, 
and in places where opportunities for establishment are greatest. Such is the case 
in the shade of the forest canopy, but where is the pioneer with such a fruit? The 
mature phase of the forest is hence the home of our large seeded tropical fruits, 
and many more live there still awaiting cultivation; destroy the forest and this 
bounty will be lost. 


Stout, pithy-stemmed, unbranching and monocarpic trees, with a terminal inflores- 
cence. Such a habit and reproductive strategy still occurs in some palms and other 
monocotyledons, but is rare among dicotyledons. The polygamodioecious tree-ivy 
Harmsiopanax of New Guinea is one example. It is a semigregarious treelet with 
huge pinnatisect leaves, of mid-mountain glades. As a nomad, however, it 
produces an abundance of flowers and small fruit as do such monocarpic palms. A 
large fruited monocarpic progenitor could only maintain cross-pollination, and 
hence the genetic variability for further continued evolution, by growing in 


19 


20 Gardens’ Bulletin, Singapore — XX1X (1976) 


gregarious stands; each unbranching treelet would thus be analogous to the 
monocarpic stems of the rhizomatous branching sago-palm Metroxylon. A stout 
pithy stem is the perfect adaptation to the unbranched monocarpic habit; The 
tube as a supporting structure is cheap and provides adequate tensile strength for 
a vertical member in a windless environment; while, as every Melanau sago 
farmer knows, the pithy core, which in dicotyledons expands as the apex enlarges 
(eg. Mabberley, 1974b), is the bank where insoluble polysaccharides gradually 
accrete until, in a flamboyant vegetable sneeze, they are converted to soluble sugars 
and surge up the giant terminal inflorescence into the developing flowers and fruits. 
The biochemistry of durianology demands further attention! 


Large pinnate leaves borne spirally with short internodes. Givnish has elegantly 
defined the adaptive significance of leaf size and shape: large entire leaves are 
structurally and photosynthetically efficient individually, but carry a high heat load 
and are therefore expensive on water resources. They more completely exclude light 
beneath than small leaves do and thus reduce the leaf area index. Pinnate leaves 
comprise small leafy organs borne on deciduous twigs; when arranged in dense 
spirals they will still cast the deep shade of large entire leaves yet bear a lesser heat 
load. Evergreen trees with large thin leaves, whether entire or variously divided and 
in dense spirals, are confined to well-watered habitats even in the humid tropics. 
Some, such as the pinnate-leaved Chisocheton and pinnatisect Heliciopsis are in 
the forest understorey and bear large, usually dehiscent fruits; here, as Givnish 
points out, the large thin leaf is advantageous on the ‘gamblers ruin’ principle, by 
spreading a given number of chloroplasts horizontally the chance of encountering 
sunflecks is increased. Others, such as the small fruited tree-ivies Harmsiopanax 
and Arthrophyllum skirt the forest fringe on river banks and in gaps. Here large 
rapidly transpiring leaves, which prevail among nomad trees of well-watered places, 
provide the most economic means of building a photosynthesizing mantle for 
rapid growth and at the same time cast deep shade, deterring competition. In a 
densely spirally pinnate-leaved slow-growing tree the latter advantage is still 
conferred, as anyone who has rested in the uncluttered shade of Dracontomelum 
mangiferum Bl. on a Bornean river bank will remember with gratitude. 


If now we add a massive inflorescence of large actinomorphic magnoliaceous 
flowers, with weakly differentiated perianth and many centrifugal stamens, we 
further define our plant’s ecology. Such flowers are a crude means of ensuring cross- 
pollination, unless self-incompatable. They are expensive to produce, and the 
greater part of the costly pollen will be wasted, unless the trees are gregarious 
which, as we have already suggested, they probably were, or the flowers conspicuous 
and the vectors specific and far-roaming. The simple thin-walled short-lived pollen 
grain so common among still existing primitive families has, like the fruit, confined 
them to habitats where the atmosphere is warm and humid at least during the 
flowering season. 


The stage may now be set for the reenactment of angiosperm evolution: we 
can visualise hills clothed in tall Araucaria forest; ferns grow in the deep shade 
beneath, while Cycadophytes and Caytoniales occupy the open fringes, along rocky 
tidges and in swampy plains. The gap phase of the Araucaria forest would have 
lacked the fast growing opportunists of modern rain forests. Here, on moist stable 
fertile slopes, hence especially on basic volcanic soils, the protoangiosperm would 
have found its niche; from a massive seed a tall shoot rapidly overtopped its 
gymnosperm seedling competitors in the shafts of light penetrating the crowns of 
ageing giants, allowing the building of the light-excluding schopf of densely spiral 
large pinnate leaves. Only its own kind could survive beneath its shade, and thus 
small, temporarily isolated but eventually expanding and coalescing, gregarious 
stands would accumulate on these slopes. These short unbranched trees hence 
excluded gymnosperms from the most favourable sites by depriving them of 
suitable conditions for establishment. This remains the secret of angiosperm 


Ecology and the Durian Theory 21 


success, and even now it is the gymnosperms which, if allowed to, can finally 
achieve the greater growth and stature, as the dwarfing of New Guinean angiosperm 
forest by the scattered araucarias still witnesses. 


Here then are the perfect conditions for further evolution and diversification: 
small gregarious colonies with few flowers and free cross-pollination, temporarily 
isolated along the slopes and thus allowing rapid local diversification; yet each 
valley, and each mountain chain, more permanently isolated. The significance of 
animal dispersal now becomes apparent. 


The evolution of the enclosed seed in an eventually dehiscing fruit is seen, 
then, not to be a response to increasing aridity, for which there is little evidence in 
the upper Jurassic-lower Cretaceous period of continental drift, but for the need 
to develop a protective covering for the enlarged endosperm until the seed is ready 
to germinate. 


Why should not cycads have accomplished the same? On the upper slopes of 
Susungdalaga in Camarines Sur, Luzon, I have seen Cycas circinalis L. growing 
in forest shade on volcanic soils. Their leaflets were sparse and their crowns 
diffuse; perhaps their less evolved vascular system and physiology prevents them 
from rapidly building and subsequently maintaining the dense excluding crown 
of the primitive angiosperm? 

Thus the first flowering plants, not gymnosperms, would have provided the 
environment in which their further evolution could occur. Only angiosperms could 
survive beneath their own shade and hence only angiosperms could eventually 
overtop them. The Durian Theory provides a morphological means by which this 
could be accomplished. This increase in diversity of tree habit would initially have 
been the main source of increased species diversity in the forest, which in itself 
necessitated greater subsequent fruit production to overcome declining opportunities 
for establishment as interspecific competition increased, and led to the extinction 
of the large-fruited monocarpic ancestors. The evolution within the rain forest of 
more flexibly arranged, smaller, leaves would also allow a further spread of 
angiosperm hegemony into the domain of gymnosperms. Yet the sparsely branching 
protoangiospermous habit and spiral divided leaves still retain their advantage in 
the forest shade and many modern leptocauls, including a Philippine Knema 
(Myristicaceae) and a New Guinea Sloanea (Elaeocarpaceae) with durian-like 
fruit, retain this habit as saplings, as Corner has noted in other forest trees. 


The evolutionary sequence of early angiospermous forest is partly reenacted 
in modern seral succession on moist hillsides. The seeds of modern forest nomads 
are small, with little food-store, and germinate in response to light but, once 
germinated the saplings rapidly build a tortoise-shell of large overlapping leaves, 
expanded by the early formation of ascending pithy shoots; among them are 
microsperm pachycauls such as Senecio mannii Hook. f. (illustrated by Mabberley 
(1974a) ). This at first, if complete, can effectively deter competition but after a 
few years the stems and branches begin to open under their own weight, providing 
the setting for the next stage, which will involve the first true leptocauls. Among 
them though, and particularly on these well watered sites, the pagoda tree (Corner, 
1940) comes to predominate, an ingenious compromise between pachycaul and 
leptocaul and probably ancient. This, by intermittent rapid extension of a stout 
pithy leader grows first into a tall unbranched sapling with spiral or whorled 
leaves; but then, after a period of dormancy, it sprouts a whorl or pseudowhorl of 
more or less horizontal branches around the apex, bearing dense ascending 
rosettes, typically of obovate leaves by Terminalia branching (Corner, 1940). Thus 
an aerial blanket of leaves, often large and presumably rapidly metabolizing is 
early formed which overtops and suppresses its many-stemmed predecessors and, 
by successive bold extensions, apical dominance is maintained until the final forest 
canopy is reached. Only then does apical dominance give way to allow the expansion 
of a dome-shaped sympodial crown, often associated with a decline in the size 


22 Gardens’ Bulletin, Singapore — X XIX (1976) 


and density of the leaves and twigs. The ascending spires of Alstonia, Terminalia, 
Bombax, Endospermum, Tetrameles and Octomeles proclaim such a stage in the 
forest cycle. Meanwhile other truly leptocaul species are establishing beneath to 
fill in the forest frame. 


It can be seen then that, first, the complexity of mature phase forest structure 
must have been formed; this also by its nature provided obstacles to cross-pollina- 
tion, and thus initiated the evolutionary sequence of floral specialization and 
diversification by which our modern families are distinguished. 


Meanwhile also, microsperm pachycauls evolved into the gap phase of the 
forest and the alpine forest fringe, and the differing conditions for reproduction 
there led to the origin of such other taxa as Senecio and Lobelia (Mabberley, 
1973, 1974c) and eventually herbaceous forms. 


It is now apparent why the Myristicaceae, primitive in so many respects and 
with primitive arillate fruit, have nevertheless developed the leptocaul habit with 
small leaves and plagiotropic branching, and flowers which are small, much reduced 
and borne on dioecious trees. Here is a family that has evolved with the forest 
from earliest times: first the fruit, then further evolution of the habit, and sub- 
sequently the flower while the earlier evolved fruit and habit continue to retain 
their adaptive advantage in the shade of the storied modern forest. But the 
Myristicaceae, as Corner points out, are tied to the rainforest by their fruit; fell 
the forest and they do not return. 


As the origin of the primitive angiospermous fruit must be interdependent 
with the early evolution of vertebrate vectors, birds and mammals, so the evolution 
of the structure of the angiospermous rain forest-not by coevolution this time but 
in response to previous vegetational change-provided the means for their rapid 
diversification. Animal diversity, once thus initiated, in turn enhanced the coevolu- 
tion of flowers and their pollen vectors, of plant hosts and their predators, which 
still continues and defines the modern complexity, long after the possibilities of 
structure, habit and leaf design had been exhausted and retained or repeated by 
many families. 


In geological time the disposition of land masses has changed, and the area 
occupied by different climates, but the range of climates and soils can rarely have 
changed. Life itself provides the changing scene. Evolution of species and phyla 
proceeds from what has already evolved before; similarly it is in those habitats 
where biotic change has been greatest that we should expect major paths of further 
evolution to originate, not in the deserts or the mountains but in the lowland forests 
especially those of the humid tropics. 


Why, then, do we find monocarpic pachycauls prevailing in the paramo, and 
the massive primitive flower more often in the mountains than the lowlands? 
Evolution has proceeded outwards from the lowland forests where only the ancient 
fruit and pinnate leaves have sometimes survived the palimpsest of subsequent 
biotic change in the understorey. But the paramo retains the moist open conditions 
of the primitive angiosperm forest while the pachycaul stem is preadapted to 
year-round frost (Mabberley 1973, 1974a) and the structural simplicity of the 
montane forest, though derived and leptocaul, allows the survival of clumsy 
pollination systems. 7 


It is therefore naive to conjecture the centre of angiosperm origin from 
modern distributions. Besides, great changes in the distribution of climates have 
occurred since the Jurassic, necessitating massive migration if not always extinction; 
even in South-East Asia Muller has shown that temperate species prevailed, 
presumably on long-vanished mountains, during the Miocene. 


Similarly, plants only fossilize under restricted conditions. The most primitive 
pollen types appear not to fossilize well and it is likely anyway that plant, and 
possibly also fruit, form diversified both within the rainforest and into other 


Ecology and the Durian Theory 23 


environments largely before flower and pollen diversification. Recent fossil evidence 
is therefore likely to be misleading. Using the Durian Theory as a basis for predic- 
tion we should pursue a different approach and should consciously search out 
volcanic ash deposits rather than riverine, swamp or aquatic, from the western 
tropical margins of the great late Jurassic oceans. If they do not exist, or bear no 
fossils, the origin of the angiosperms will remain enigmatic. 


REFERENCES 


CORNER, E. J. H. 1940. Wayside Trees of Malaya. Vol. I: 770 pp; vol. II: 
228 pl. Government Printing Office, Singapore. 


1949. The Durian Theory or the origin of the modern tree. Ann. Bot. 
(N.S.) 13: 367-414. 


1953. The Durian Theory extended — I. Phytomorphology 3: 
465-476. 


1954a, The Durian Theory extended — II. The arillate fruit and the 
compound leaf. Phytomorphology 4: 152-165. 


1954b. The Durian Theory extended — III. Pachycauly and 
megaspermy — Conclusion. Phytomorphology 4: 263-274. 


1964. The Life of Plants. Pp. 315 + 41 pl. Weidenfeld & Nicholson, 
London. 


GIVNISH, T. J. 1975. Ecological aspects of plant morphology. Unpublished MS 
of paper delivered at XII International Botanical Congress, Leningrad 
(Abstract in [A. Takhtajan], Abstracts of the papers presented at the XII 
International Botanical Congress, July 3-10, 1975, 1: 214). 


MABBERLEY, D. J. 1973. Evolution in the Giant Groundsels. Kew Bull. 28: 
61-96. 


1974a. Branching in pachycaul Senecios: the Durian Theory and the 
evolution of angiospermous trees and herbs. New Phytol. 73: 967-975. 


1974b. Pachycauly, vessel-elements, islands and the evolution of 
arborescence in ‘herbaceous’ families. New Phytol. 73: 977-984. 


1974c. The pachycaul Lobelias of Africa and St. Helena. Kew Bull. 
29: 535-584. 


MULLER, J. 1966. Montane pollen from the Tertiary of N. W. Borneo. Blumea 
14: 231-235. 


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The Reproductive Biology of Durio zibethinus Murr. 


by 
E. SOEPADMO & B. K. EOW 


Department of Botany, University of Malaya 


Kuala Lumpur 


SUMMARY 


Durio zibethinus Murr. or the common durian is a fruit-tree species widely cultivated 
in villages or orchards or a semi-wild plant found growing around aborigines’ settlements 
in Peninsular Malaysia. The species is generally considered by botanists as a native tree in 
Borneo and Sumatra, though currently it is commonly planted throughout South East Asia, 
extending from the south-eastern parts of India to New Guinea. 


In Peninsular Malaysia the flowering is seasonal and normally falls during the months 
of March-April and September-October, though accessory flowering may take place in between. 
Development of flowers takes about five to seven weeks and the flowering lasts for about 
three weeks. Floral parts develop acropetally and the epicalyx, calyx, corolla and stamens 
fall off soon after anthesis. Floral anthesis is initiated at about 16.00 hrs. and completed by 
about 20.00 hrs. Pollination is carried out by nectarivorous bats (Eonycteris spelaea) and by 
an unidentified noctuid moth, and takes place between 20.00 and 01.00 hrs. Pollen grains 
are more or less spherical, 80-150 , in diameter, 3-4- or rarely 6-porate, with a smooth but 
sticky exine; kept under room temperature they remain viable for about 48 hrs. The flower 
is self-compatible, though the percentage of successful fertilisation and production of fruit 
reaching maturity increase if the flowers are crossed. 


The anthers though initially tetrasporangiate become bisporangiate at maturity. Wall 
development conforms with the basic type. Before anthesis the epidermis is made up of more 
or less rectangular and isodiametric cells, but towards anthesis these cells become papillate 
and filled with tannin, and eventually shed off from the anther wall. The endothecial cells 
become fibrous and both the middle layers and the tapetal layer are crushed and disappear, 
leaving the endothecium the only wall enclosing the pollen grains. Cytokinesis of microspore 
mother cells is simultaneous and gives rise to tetrahedral tetrads. Anther dehiscense is 
through a longitudinal slit caused by the breakdown of the wall at the meeting point of the 
anther-lobes. Pollen grains are binucleate at the time of shedding. 


__ The ovule is anatropous, bitegmic and crassinucellate. The micropyle is formed by both 
anal at Embryo-sac development conforms with the Polygonum-type. Antipodal cells are 
ephemera 


The seed is arillate and its mode of germination is epigeal and takes place within three 
days after sowing in garden soil. Seed viability can be prolonged up to 32 days (90% 
oo if the seeds are surface-sterilised, kept in an air-tight container and placed under 

°C. 


INTRODUCTION 


Previous works on Durio (Wyatt-Smith, 1953; Kostermans, 1958; Reksodi- 
hardjo, 1962 and Kochummen, 1972) indicate that there are at least 28 species in 
the genus, distributed throughout Burma, Thailand, Peninsular Malaysia, Singapore. 
Sumatra, Borneo and Palawan Island. Though considered by botanists as a tree 
native to Sumatra and Borneo, Durio zibethinus or the common durian is now 
widely cultivated as a fruit-tree in the South Asia region, covering the south-eastern 
parts of India, Ceylon, Burma, Thailand, Indo-china, Malaysia, Singapore. 
Indonesia, the Philippines and New Guinea. 


Species of Durio are found growing naturally in lowland and hill primary 
forests (up to 1000 m altitude) usually not more than 3 to 4 trees per hectare. 
Apart from Durio zibethinus there are five other species which produce edible 


25 


26 Gardens’ Bulletin, Singapore —- X XIX (1976) 


fruits (Reksodihardjo, 1962). These are D. dulcis Becc. (found in Sabah and 
Indonesian Borneo), D. grandiflorus (Mast.)Kost. (Sabah, Sarawak and the Indo- 
nesian Borneo), D. graveolens Becc. (Peninsular Malaysia, throughout Borneo and 
Sumatra), D. kutejensis (Hassk.) Becc. (throughout Borneo), and D. oxleyanus 
Griff. (Peninsular Malaysia, throughout Borneo and Sumatra). All five are culti- 
vated in Brunei and some to a limited extent elsewhere in Malaysian Borneo. The 
other species of the genus, though not producing edible fruits, possess several 
desirable features for breeding and bud-grafting purposes. These features are: 
disease and pest resistance (most wild species), more regular flowering (D. acuti- 
folius (Mast.) Kost. & D. griffithii (Mast.) Bakh.), flowers and fruits borne on the 
lower parts of the stem (D. beccarianus Kost. & Soeg., pinangianus (Becc.) Ridl. 
and testudinarum Becc.), or on the stem as well as on the lower branches (D. 
malaccensis Mast.). Though this does not necessarily mean that all species are 
easily hybridised, it does imply that, since the specific delimitation of the genus is 
mainly based on morphological attributes and since there are several species which 
are closely related to each other (e.g. D. zibethinus, malaccensis and wyatt-smithii 
Kost.), and, there seem to be many intermediate forms among natural populations 
of and between species, there is a possibility to improve the quality as well as the 
productivity of the existing edible-fruit producing species, at least by bud-grafting. 


In spite of the fact that durian fruit is of high economic importance to local 
inhabitants (Lai, 1974), as far as we know there is no large scale plantation or 
estate in the region, nor is there a well documented and systematic breeding and 
selection programme, This lack of interest may partly be due to the fact that very 
little is known about the autecology, flowering biology, cytology and breeding 
system of the species. The only paper dealing with some aspects of reproductive 
biology of Durio species so far published is that by Valvayor, Coronel & Ramirez 
in 1965. 


It is therefore the aim of the present study to gather more information about 
D. zibethinus and its related species so that their economic potential and contribu- 
tion to “durianology” in general is not completely forgotten. 


MATERIALS & METHODS 


Field work to determine the distribution and frequency and to observe the 
phenology, floral anthesis and pollination processes of D. zibethinus and its related 
species was carried out in the University of Malaya campus, Damansara village, 
Ulu Gombak, Mantin and Kuala Selangor (all in Selangor State), Kuala Pilah and 
Pasoh Forest Reserve (in Negri Sembilan), Krau Game Reserve, Taman Negara 
and Tioman Island (Pahang). For detailed studies on the floral anthesis and for 
pollination experiments, a tree growing in the compound of the Faculty of Agri- 
culture, University of Malaya was used. 


Flowers of different developmental stages were collected regularly during the 
flowering periods, fixed in 50% F.A.A. solution and then sectioned and stained 
according to normal schedules. Guano samples were collected weekly from Cavern 
C of the Batu Caves Limestone Hill from February 1974 to January 1975, Pollen 
content was extracted from these samples and acetolysed and then stained with 
safranin. 


OBSERVATIONS & RESULTS 


Phenology. Depending on the clones, soil and climatic condition in which the 
durian tree is planted, it starts to bear flowers and fruits at the age of 5 to 12 
years, In Peninsular Malaysia there seem to be two main flowering seasons, 
normally falling in the period of March-April and September-October. However, 
it should be noted that minor or accessory flowering may occur in between, The 
flowers are born in fascicles of 3-30 on the older branches, Flowers of the same 


Durio Zibethinus, Reproductive Biology 27 


inflorescence usually mature more or less at the same time and open one after 
another within a few days. Since during the flowering each individual tree produces 
hundreds of flowers, and the maturation of the flowers of different inflorescences 
is not necessarily synchronised, the flowering period of a particular season usually 
lasts for about two or three weeks. It was also observed that normally the first 
flowering of a particular year is heavier than the second. What causes this remains 
to be investigated. The fruit set is usually very low since many of the ovaries will 
drop after anthesis, either because their ovules are not fertilised or have been 
disturbed or destroyed by the pollinators. Fruits take approximately three months 
to reach maturity. 


Floral morphology and development. At its early stage of development, each 
individual flower-bud is a globose structure made up of a mass of homogeneous 
cells surrounded and enclosed by bracts and epicalyx. The sepaline, petaline, 
staminal and carpellary primordia develop acropetally at more or less the same 
rate. The anthers develop from the distal cells of the phalanges as globular pro- 
tuberances, Each protuberance is composed of a homogeneous mass of meristematic 
cells surrounded by an epidermis. As the phalanges elongate and differentiate into 
distinct filaments the developing young anthers assume their 4-lobed appearance. 
Just before anthesis the buds attain a size of about 2 cm in diameter. Both the 
epicalyx and calyx are externally densely covered with brownish peltate fimbriate 
scales, and the petals are yellowish-white and sparsely hairy outside. The scales 
are multicellular and originate from the epidermal cells. The nectary is located at 
the inner basal part of the calyx-cup. At anthesis the flower reaches about 5-6 cm 
long and 2-3 cm in diameter and emits a strong odour reminiscent of sour milk but 
somewhat fragrant. The carpels develop and originate from a common primordium 
situated at the centre of the flower-bud. This primordium is made 
up of homogeneous and more or lesss isodiametric cells. These cells divide and 
differentiate into five carpels which fuse at their marginal and central parts to 
form a 5-loculate ovary with a central placental column. The style is formed by 
vertical growth of the five carpels and is topped by a capitate stigma. The stigmatic 
surface is uneven in outline with deep depressions or notches here and there 
(Plate 4a). By the time the megaspore mother cell is formed, the spine-primordia 
of the ovary wall start to develop. These primordia originate from the hypodermal 
layer and appear as conical protuberances each of which is topped by a multi- 
cellular, peltate and fimbriate scale similar to those of epicalyx and calyx. As the 
flower develops fully, cells in the tissues of the epicalyx, calyx and petals contain 
tannin and become mucilaginous. 


Development of anther-wall. In each of the anther lobes and just below the 
epidermis, a row of hypodermal cells increase in size and contain more conspicuous 
nuclei and denser cytoplasm. These cells form the archesporial tissue. Each 
archesporial cell divides periclinally into a primary parietal cell and a primary 
sporogenous cell (Pl. la). The primary parietal cell further divides periclinally 
into two secondary parietal cells. The outer secondary parietal cell divides once 
again to give rise to an endothecial cell and outer middle-layer cell. The inner 
secondary parietal cell also divides further and produces the inner middle-layer 
cell and the tapetal cell. Thus the anther-wall formation conforms well with the 
basic type. By the time the sporogenous cell divides and produces numerous 
microspore mother cells, the anther wall is greatly stretched and the middle layers 
as well as the tapetum are crushed and their cells become flattened. Meanwhile 
through the disintegration of the septa separating the four original anther cavities, 
the anther becomes two-loculate. Towards the end of meiosis the epidermal cells 
become papillate and filled with tannin, and just before the anther dehisces they 
are shed off leaving the endothecial cells as the only surviving wall enclosing the 
pollen grains. At this stage the wall of the endothecial cells becomes fibrous and 
the wall thickening appears as radially oriented bar-like structures. 


28 Gardens’ Bulletin, Singapore — XX1X (1976) 


Microsporogenesis. By the time the anther wall attains its 4-cells thickness, 
the primary sporogenous cell divides into two daughter cells (Plate 1b). These cells 
divide both periclinally and anticlinally to form numerous microspore mother 
cells (Plate 1c & d). Meiotic division starts from those microspore mother cells 
situated at the centre of the anther cavity and progresses outwards (Plate le & f). 
Many of the peripheral microspore mother cells fail to complete the division and 
become abortive and assume a flat outline. The first division of the microspore 
mother cell is not immediately followed by wall formation (Plate le). The 
resulting four microspores are formed simultaneously and clustered in a tetrahedral 
arrangement (Plate 1f). At the time of shedding most of the pollen grains are 
binucleate. It may be noted that development as well as formation of microspores 
are not synchronised in all anthers of the same flower. 


Pollen morphology. Mature pollen grains are more or less spherical, 3-4 rarely 
6-porate, and measuring 80-150 » in diameter (Plate 2a). The exine is very much 
thicker than the intine, smooth but covered with sticky substances, and thicker 
around the pores. At anthesis they are released singly or in clumps (Plate 2b). 


Pollen germination, Pollen grains collected from the anthers at the beginning 
of floral anthesis do not show any sign of germination, but those collected from 
the fallen phalanges on the following morning start to germinate. Two hundred of 
these pollen grains were kept under room temperature, and after 40 hours from 
23.5 to 80% of the pollen grains germinated. This seems to indicate that stigmatic 
exudate is not the sole prerequisite of germination and that kept under room 
temperature the pollen remain viable for at least 48 hours. Germination experiment 
using sucrose solution of various concentrations shows that after culturing the pollen 
for 12 hours, the optimal percentage of germination (c. 77%) takes place in 
6% solution, In this experiment it was also observed that the higher the concentra- 
tion of the sucrose, the longer the pollen-tube is. 


Development of ovule. In each of the carpellary cavities two alternate rows 
of 5-7 ovular primordia appear from the central placental column as minute and 
somewhat conical protuberances (Plate 2c). Each primordium is at first composed 
of homogeneous, thin-walled and more or less isodiametric cells, but later one of 
the hypodermal cells becomes larger in size than the surrounding cells and contains 
dense cytoplasm and a more conspicuous nucleus (Plate 2c). This cell develops 
into the archesporial cell and divides periclinally into a primary parietal cell and 
sporogenous cell (Plate 2c). The primary parietal cell divides periclinally and 
anticlinally to form the 5-6 cells thick nucellus. Soon after the division of arches- 
porial cells is completed, the integument primordia develop more or less simul- 
taneously on both sides of the nucellus (Plate 2d). However, the outer integument 
grows faster and eventually overtops the inner one. The micropyle is formed by 
both the inner and outer integuments. At the formation of the megaspore mother 
cell the integuments are 2-3 cells thick, and later more cells are laid down. Several 
cells of the outer integument are eventually filled with tannin. It may be noted here 
that on two occasions binucellate ovules were observed. The two nucelli are 
enclosed by a common outer integument but each has its own inner integument. 


Megasporogenesis. The sporogenous cell enlarges and functions as the megas- 
pore mother cell (Plate 2d). This cell divides into two (not seen) and eventually 
into four daughter cells arranged in a linear tetrad (Plate 2e). Three of these 
daughter cells degenerate, leaving the cell at the chalazal end to develop further. 
This functional megaspore undergoes vacuolation and forms an _ elongated 
uninucleate embryo-sac. Subsequently it passes through two-, four-— and eight- 
nucleate stages before cytokinesis commences (Plate 3a, b & c). One of the four 
micropylar daughter nuclei moves towards the centre of the embryo-sac, and the 
other three form the egg apparatus and two synergids. Similarly, one of the 
chalazal nuclei also moves to the centre of the embryo-sac while the other three 
form the ephemeral antipodals (Plate 3c & d). The two polar nuclei then fuse 


Durio Zibethinus, Reproductive Biology 29 


with one another to form the secondary polar nucleus (Plates 4c & 5a). The 
development of the eight-nucleate embryo-sac, therefore, conforms well with the 
Polygonum-type. 


Pollination, Opening of the flower usually takes place according to the following 
sequence: epicalyx splits into 2-3 ovate-concave lobes about 12-24 hours before 
anthesis; the calyx then splits open at its tip into 5—6 acute lobes about 8-10 hours 
before anthesis; for the next two hours or so the petals, styles and stamens which 
initially take an incurved position within the calyx become fully exerted and soon 
after dark the petal-lobes become recurved outwards exposing both stamens and 
styles; meanwhile some of the anthers may start to dehisce but the majority do 
not do so before c. 19.30 hrs; the stigmatic surface becomes receptive at about 
20.00 hrs. The flower remains at this stage until about 01.00 hrs., and then the 
calyx, petals and stamens begin to drop off, leaving the lone ovary remains 
attached to the branch. Though initially many of these ovaries remain attached 
to the branch following pollination, within a few days most of them drop off and 
leave only 1-2 per inflorescence. 


During the late afternoon, the flowers are visited by various insects as they 
open. Among these are honey bees, house-flies, lady-bird beetles, scarab beetles, 
and lacewings. Pollen grains were found on the legs and bodies of these insects but 
not in their guts. Since these insects visit the flowers before the latter reach full 
anthesis, they cannot be considered as pollinators. In the evening, namely between 
20.00 and 01.00 hrs, the flowers are visited by three different species of bats. These 
are the nectarivorous bat (Eonycteris spelaea) and the frugivorous bats Cynop- 
terus brachyotis and Pteropus vampyrus. Occasionally nocturnal moths also visit 
the flowers during this period. Among the bats, only Eonycteris spelaea could be 
considered as the genuine pollinator, since the other two directly feed on and chew 
up the flowers (Start, 1974). Our observation suggests that Eonycteris spelaea feeds 
on nectar as well as on pollen grains, and it does not chew the flower. The bats 
also visit the flowers regularly during the flowering season; they land on and 
clutch the flowers with the frontal parts of their body facing the open flowers. 
Analysis of guano samples also confirms that pollen grain of Durio zibethinus 
constitutes a significant part of the bat’s diet during durian flowering season and 
that the highest number of grains in the samples coincides well with the flowering 
season of the trees. Other important pollen grains found constantly in the guano 
samples are those of Parkia, Ceiba pentandra (L.) Gaertn., Bombax valetonii 
Hochr., Oroxylon indicum Vent., Duabanga grandiflora (Roxb. ex DC.) Walp., 
Artocarpus spp. (Plate 6a-d). This suggests that the bats feed on nectar or pollen, 
or both, of different species of plants which flower at different times of the year, 
and pollinate the flowers. 


Pollination experiments. To test the compatibility of the flowers, a series of 
preliminary experiments were carried out during the flowering seasons in 1974. In 
each experiment a set of 20 flowers having a similar stage of development were 
selected and tagged. These flowers were then given the following treatments: (1) 
all anthers were removed at anthesis and the stigmas were exposed to natural 
pollinators, (2) the flowers were bagged before anthesis, (3) the stigmas were 
applied with Cutex nail varnish to prevent pollination, (4) the flowers were self- 
pollinated by hand and bagged, and (5) the anthers were removed and the stigmas 
were cross-pollinated by hand with pollen of other flowers of the same tree, and 
then bagged. At the beginning of these experiments the ovaries of all flowers used 
were between 0.35 and 0.4 cm in diameter and light-brown in colour, After 5 days 
all tagged flowers were re-examined and the following results were obtained: in 
treatment no. 1, 45% of the ovaries remained attached to the branch and showed 
further development, i.e. increase in diameter (0.50.6 cm) and change in colour 
to olive green; in experiment no. 2, only 15% of the ovaries showed further sign 
of development and the others either shrivelled or fell off; in the 3rd treatment 


30 Gardens’ Bulletin, Singapore — X X1X (1976) 


none of the ovaries underwent further development and shrivelled or dropped 
off: in the 4th, 50% of the ovaries exhibited further development and remained 
attached to the branch; and in the Sth 65% of the ovaries underwent further 
development and remained attached to the branch. At the end of the flowering 
season only 5% of the successfully pollinated ovaries developed into mature fruits. 

The above experiments seem to suggest that (i) natural pollinators contribute 
at least 45% of the successful pollination, (ii) natural self-pollination can take 
place and contribute to 15% successful pollination, (iii) pollination is a pre- 
requisite of fruit development, (iv) up to 50% of the flowers are self-compatible, and 
(v) cross-pollination between flowers of the same tree is the better means for 
successful fertilisation and eventual fruit development. 

However, it should be emphasised here that since the number of flowers used 
in the experiments is small and the work was conducted on a single tree only, the 
above mentioned results should be considered as tentative. Future experiments 
using larger number of flowers and trees will either confirm or contradict the 
above results. 

Fertilisation. The receptive stigma is heavily papillate and has a glistening and 
sticky surface. Pollen grains deposited on the stigmatic surface germinate within 3 
or 4 hours. The germinating pollen grains are mostly monosiphonous, and the 
tubes make their way through the stigmatic papillae into the style. The pollen tubes 
grow downwards through the intercellular spaces of the vertically elongated 
protoplasmic cells of the transmitting tissue (Plate 4b). The successful tube enters 
the embryo-sac through the micropyle (Plate 4d). Although hundreds of slides were 
examined by us, the actual process of fertilisation has not been observed in detail. 
From the specimens available it seems that just before fertilisation the secondary 
polar nucleus moves nearer to the egg apparatus (Plates 4e & Sa). 

Endosperm. The secondary polar nucleus which is situated near to the egg 
apparatus is then fertilised by one of the male gametes to form the primary 
endosperm cell (Plate 5a). This cell enlarges and undergoes free nuclear division. 
Most of the nuclei produced are distributed along the periphery of the embryo-sac 
and aggregated mainly at the chalazal end (Plate 5b). The endosperm remains in 
a free nuclear condition until a late stage of embryogeny and then becomes 
cellular. 

Development of embryo and seed. In the present study the embryogeny has 
not been followed in detail. Sections of developing seed indicate that the endosperm 
does not persist and the cotyledons occupy the greater part of the seed cavity. The 
starchy food reserve is therefore stored in the cotyledons. Cells of the inner 
integument are crushed and disappear, and those of the outer integument become 
fibrous with the epidermal cells developing into rectangular and heavily lignified 
stone cells each with a very small lumen. The aril develops from the funicular end 
and eventually completely encloses the seed. This aril is very variable in thickness, 
colour, taste, smell and moisture content. It may be noted here that in a few clones, 
there is a high incidence of seed abortion, in which the seeds shrivel and measure 
less than 4 by 1.5 cm, while fully developed and viable seeds measure up to 
7 by 4 cm. 

Seed germination, The first sign of germination is indicated by cracking of the 
hilum at the micropylar end, and this takes place within 3 to 4 days after sowing 
the seeds in suitable medium. The radicle will emerge from this crack, elongate 
and grow downwards, After approximately 10 days numerous lateral roots appear 
at the proximal end of the radicle and the hypocotyl elongates and straightens 
up bringing the cotyledons still enclosed by the testa slightly above the soil surface. 
Subsequently the petioles or stalks of the cotyledons elongate allowing the plumule 
to emerge. The plumule elongates and from it the first and second leaves appear. 
These leaves are much smaller than the normal leaves and are deciduous. The 
cotyledons shrivel and drop off within 38 days following germination. 


Plate 1: a & b developing anthers with sporogenous cell (spc); c & d dividing and developing 
microspore mother cells (mc); e division of microspore mother cells; f end of 
meiosis and formation of pollen tetrads (ptr). 


ronennene nnn meni nay 


Plate 2: a & b cross-sections of anthers just before anthesis showing fibrous endothecium and 
mature pollen grains; c ovule primordium showing primary parietal cell (ppc) and : 
primary sporogenous cell (psc); d ovule primordium showing developing megaspore 
mother cell (mmc) and integuments; e linear tetrad and functional megaspore (fms). 


Plate 3: a 2-nucleate embryo-sac; b 4-nucleate embryo-sac; c & d 8-nucleate embryo-sac; 
pn = polar nuclei. 


MX 


Vif, 


es i, 
WHE, 


tity, 
Ye 


WO 
WS 
SS 


SSS 


~ 


NS 
Ss 


SS 
. 
» 


: @ longitudinal section of stigma (pg = pollen grain; pt = pollen tube); b pollen 
tube (pt) growing downwards through the stylar tissue; ¢ migration of polar nuclei 
(pn) towards micropylar end of the embryo-sac; d pollen tube (pt) entering embryo- 
sac through micropyle. 


‘(ou) wodsopuso 
Jvojonu gq suoOHesi[sJoJ oJOJoq ysnf (oud) snojonu Ivjod Arvpuosss Jo uoeuUoy PD :¢ deg 


Plate 6: a & b pollen grains extracted from guano samples (D = Durio; P = Parkia; 
Db = Duabanga grandiflora; O = Oroxylon indicum); c pollen of Durio zibethinus; 
d pollen of Bombax valetonit. 


Durio Zibethinus, Reproductive Biology 31 


Experiments show that: (i) if the aril is removed from the seedcoat, up to 
95% of the seeds tested germinate 3 days after sowing in various media (saw-dust, 
sands, and garden soil); (ii) if the aril is not removed, only 40% of the seeds 
begin to show signs of germination 6 days after sowing, and to reach 95% 
germination rate, 10 days after sowing is required; (iii) though initially there 
seems to be no significant difference in percentage of germination, for further growth 
of seedlings the garden soil is the best medium; (iv) the average moisture content 
of a fresh seed is c. 51% (wt). Kept under room temperature (36°C) the moisture 
content drops to c. 23% after 32 days of storage. If, however, the temperature is 
lowered to 20°C and the seeds are stored in an air-tight container, the moisture 
content can be kept at 43-45% level for the same length of storage time; (v) 
surface sterilised, kept in an air-tight container and stored under 20°C the seeds 
remain viable (up to 90% germination rate) for at least 32 days, but if the seeds 
are stored under 36°C they lose viability after only 6 days’ storage. 


DISCUSSION 


From the foregoing chapters it is evident that in order to understand the 
reproductive biology and the breeding system of D. zibethinus and its related 
species, and to appreciate their economic potential, more detailed studies remain 
to be carried out in the future. In particular, the questions — whether all existing 
varieties and clones are self-compatible or require cross-pollination to produce a 
good crop of fruits, and whether it is possible at all to hybridise at least the closely 
related species of the genus, etc. — remain to be clarified. 


Our observation on a single tree suggests that, in this particular clone at least, 
there is a certain degree of self-compatibility if the flowers are cross-pollinated by 
hand. This seems to disagree with the results obtained by Valmajor and his 
co-workers (1965) in the Philippines, in which they observed that all trees under 
their investigation were completely self-incompatible, and that the trees set fruits 
only if they were reciprocally cross-pollinated. However, since in Peninsular 
Malaysia alone there are at least 44 clones (Ho, 1971), differing slightly from one 
another in their fruit-yield, intensity and frequency of flowering, floral and fruit 
morphology, and quality of the aril, it is reasonable to assume that different clones 
might have different patterns of breeding system and reproduction. This assumption 
is substantiated by the fact that among the clones observed there are trees which 
have the styles shorter than the stamens and exerted from the enclosing corolla 
more or less at the same time with the stamens; and, there are those trees which 
possess styles longer than the stamens and exerted from the enclosing corolla 
before the stamens, with the stigmas thus positioned way above the anthers. Judging 
from the way the bats alight on the flowers during feeding, it seems likely that in 
the first category of clones both self-and cross-pollination are possible, whereas in 
the second case only cross-pollination can take place. Furthermore, since in the 
latter case there is a time interval intervening between the dehiscence of anthers 
and the receptivity of the stigmas, under natural condition only cross-pollination 
between flowers of the same or of different trees is possible. In this case any 
pollinator alighting on the flowers before the stigmas become receptive will not 
affect pollination, but during feeding, pollen grains of dehiscing anthers may 
get attached to the mouth and frontal parts of the pollinator’s body. In moving and 
alighting to another flower later in the evening the pollinator will brush pollen 
grains on the now receptive stigma. 


In their paper, Valmajor and his co-workers stated further that reciprocal 
cross-pollination by hand of the self-incompatible trees resulted in 87.3 to 90% 
fruit set. This is obviously a very high rate of fruit set by any standard, since at 
least in Peninsular Malaysia, 20 to 25% fruit set is generally considered as a very 
good crop already. In addition to this, our experiment also shows that up to 65% 


32 Gardens’ Bulletin, Singapore — X XIX (1976) 


successful pollination can be obtained if the flowers are cross-pollinated by hand 
with pollen grains of other flowers of the same tree. These seem to suggest that 
if a means could be found to store and keep the pollen grains viable for a longer 
period than their natural viability, and a method could be devised to deposit pollen 
grains on the receptive stigmas efficiently, artificial pollination may turn out to be 
the best way to increase fruit production of a durian tree. 


With regard to the possibility of hybridizing at least the closely related species 
of the genus, Reksodihardjo (1962) stated that a natural hybrid between D. 
zibethinus and D. graveolens has been discovered in the north-eastern parts of the 
Indonesian Borneo. More recently, Heaslett (1972) reported that in Johore State 
he found several trees of D. malaccensis with pink- or red-tinged flowers. Since 
normally this species has a white or creamy flower, and moreover in Peninsular 
Malaysia the only species with pink or red flowers are D. lowianus King and D. 
pinangianus (Kochummen, 1972), the trees observed in the forests of Johore by 
Heaslett may yet represent another natural hybrid between parents of closely 
related species. If the status and origin of these “natural hybrids” could be 
determined and confirmed, then there is a great possibility that through a breeding 
and selection programme much improved clones could be obtained. 


Finally it is re-emphasised here that the detailed processes of fertilisation and 
embryogenesis, the significance of binucellate ovules and high incidence of seed 
abortion, and the factors affecting the development and quality of the edible aril 
also need further studies. 


ACKNOWLEDGMENTS 


We wish to express our sincere thanks to the Vice Chancellor of the University 
of Malaya and to the Director of the Malaysian Agricultural Research and 
Development Institute (MARDI) for the research grants which made the present 
work possible. 


We are also very grateful to Dr. N. Prakash for his kind cooperation and help 
given during the execution of this work and to Dr, P. S. Ashton for his constructive 
criticisms on the manuscript. For their technical assistance we are very much 
obliged to Mrs. Babe Foo and Mr. Mahmud bin Sider. 


Finally we would like to thank Prof, E. J. H. Corner for his continual interest 
and encouragement extended to us in pursuing works on tropical plants. 


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CORNER, E. J. H. 1949. The Durian Theory or the origin of the modern tree. 
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1952. Wayside Trees of Malaya. 2nd ed., vol. 1, 437-440. Govern- 
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—————— 1953. The durian theory extended. Phytomorphology 3: 465-476; 
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Durio Zibethinus, Reproductive Biology 33 


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3: 357-460. 


LAI, ANDREW K. K. 1974. The economics of establishing a 400-acre fruit 
orchard in Peninsular Malaysia. Malay. agric. J.: 49: 421-432. 


MEIJER, W. 1969. Fruit trees in Sabah (North Borneo). Malay. Forester 32: 
252-265. 


NG; F. ra Peay Germination of fresh seeds of Malaysian trees. Malay. Forester 
: 54-65. 


NG, F. S. P. & H. S. LOW, 1974. Flowering to fruiting periods of Malaysian Trees. 
Malay. Forester 37: 127-132. 


OCHSE, J. J. & R. C. BAKHUIZEN v.d. BRINK Sr. 1931. Fruits and fruit 
cultures in the Dutch East Indies. pp. 27-30. 


REKSODIHARDIJO, W. S. 1962. The species of Durio with edible fruits. Econ. 
Bot. 16: 270-282. 


START, A. N. 1974. The feeding biology in relation to food source of nectarivorous 
bats (Chiroptera: Macroglossinae) in Malaysia. Unpublished Ph. D. Thesis, 
Department of Zoology, University of Aberdeen, Scotland. 


VALMAJOR, R. V., R. E. CORONEL & D. A. RAMIREZ, 1965. Studies on floral 
biology, fruit set and fruit development in Durian. Philipp. Agric. 47: 355-366. 


WYATT-SMITH, J. 1954. Materials for a revision of Malayan Durio with notes 
on Bornean species. Kew Bull.: 513-532. 


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The Syncarp of Artocarpus — a unique biological phenomenon 


by 
FRANCES M. JARRETT 


Royal Botanic Gardens, Kew 


The unique compound fruit or syncarp of Artocarpus is a fascinating object 
of study, both for its basic morphology and for its structural and functional 
diversity. The opportunity that was given to me as a student of Professor Corner 
to continue his studies on Artocarpus and carry out a revision of the genus (Jarrett 
1959a, 1959b, 1960) is one that I shall always appreciate. In honouring him in this 
volume it may be of value to provide a general consideration of the syncarp, 
drawing together facts that became somewhat scattered in my monograph. The 
insights into both its internal structure and its biological significance originated 
with Professor Corner. The revisionary work extended knowledge of the syncarp 
structure to nearly all species of the genus and made it possible to place the varia- 
tions observed in a more detailed taxonomic framework. 


If one turns first to the morphology, it is found that in Artocarpus the com- 
pound inflorescence of the Moraceae is condensed into capitate, unisexual inflores- 
cences in which each of the numerous perianths contains a single stamen or ovary. 
In the male inflorescence the perianths remain free (as they do in both sexes in the 
allied genus Prainea) but in the female head the perianths are more or less com- 
pletely fused. Where the fusion is only partial it occurs in a highly specialized 
manner, which is not evident until the syncarp is dissected. It can then be seen that 
each perianth has a proximal free tubular region with a broad lumen enclosing 
the ovary. Distally, however, the perianths are early adnate to their neighbours, 
either fusing with them completely or leaving the perianth apex free. They thus 
form a continuous external wall to the syncarp which has considerable mechanical 
strength and is pierced only by the narrow lumen in each perianth through which 
the style is exserted. Passing from the axis to the outer surface, each perianth thus 
has either two or three zones, free—fused or free—fused—free. The latter condition 
was illustrated by Corner (1939) for A. integer (Thunb.) Merr. and A. hetero- 
phyllus Lam. The varying internal structure of the syncarp and some aspects of 
its external appearance are illustrated below. 


In other species, however, the fusion between the perianths is complete or, 
alternatively, it may be said that the ovaries are enclosed in cavities in a receptacle 
in which axial and floral elements are not clearly distinguishable. 


This then is the basic structure of the compound syncarp of Artocarpus, but 
such a highly specialized and apparently restrictive ground plan can, nevertheless, 
allow considerable morphological and biological diversity, especially in those 
species in which the perianths remain free proximally. Monographic study of 
Artocarpus showed that these variations could be linked with the taxonomic sub- 
division of the genus in which other characters, especially details of leaf anatomy, 
were taken into consideration, although it also became evident that some parallel 
evolution had occurred in the syncarp. 


Thus a primary taxonomic subdivision into two subgenera, Artocarpus and 
Pseudojaca, which can readily be made on the basis of spirally arranged versus 
alternate and distichous leaves, and amplexicaul versus lateral stipules, can be 


35 


36 Gardens’ Bulletin, Singapore — X XIX (1976) 


ee a ae et ee et ee a 


S 
LFF 
LH} 


\, «AY 
( 
cue 
*, Wr eeet te, 
im a . 
: > 
as 


eet cons: g 


Fig. 1. The syncarp in Artocarpus. Subg. Artocarpus. A. hispidus. a, b, longitudinal section 
and tangential section in plane x-y at anthesis, X 10; c, longitudinal section at maturity, 
x 4; d, part of the same (1, fruiting perianth; 2, ovary; 3, testa; 4, umexpanded perianth), 
xX 1. A. elasticus. e, submature head, X 4. Subg. Pseudojaca. A. peltatus Merr. f, oblique 
section at anthesis (perianths free proximally), X 24; g; longitudinal section at maturity, X 4. 
A. fulvicortex Jarrett. h, oblique section at anthesis (perianths completely fused), X 1; i, part 
of the same, X 3. a-—d redrawn from Jarrett (1959a). 


correlated quite closely with syncarp characters, In subg. Artocarpus the syncarp 
is usually ellipsoid or cylindric and the perianths are nearly always free both 
proximally and at the apex. Most species can in fact be identified by the perianth 
apices alone (cf. Jarrett, 1959b, f. 16). In subg. Pseudojaca, on the other hand, 
the syncarp is much more uniform in appearance. It is either subglobose or 
shallowly lobed with a smooth or papillate surface and although in most species 
the perianths are free proximally, there are several in which they are completely 
fused. 


Artocar pus subg. Artocarpus was further subdivided (Jarrett, 1959b) into two 
sections based mainly on characters of the inflorescence, including those of the 
embryo, and into several series based primarily, though not solely, on the distinc- 
tive, microscopic, capitate hairs on the leaves. Considered biologically and morpho- 
logically, three different syncarp types can be recognised in the subgenus corres- 
ponding with one or more of these taxonomic subdivisions, while subg. Pseudojaca 
forms a fourth type to which three species from subg. Artocarpus (ser. Rugosi) 
should also be referred. 


The biological evolution of the syncarp has apparently proceeded in two 
different directions. It is, of course, indehiscent and is broken down only by the 
frugiferous mammals and birds that feed upon it or by decay. Nevertheless it can 
be attractive either as a whole, if the entire syncarp is more or less fleshy, or for 
the individual fruiting perianths in species where the free proximal region of the 
perianth is hypertrophied. 


Syncarp of Artocarpus 37 


The least specialized condition of the syncarp would seem to be found in a 
number of species in subg. Artocarpus sect. Artocarpus in which the distal regions 
of the perianths forming the external wall of the syncarp and the free perianth 
apices are fleshy but more or less firm while the free proximal regions are thin- 
walled or only slightly hypertrophied (but sweet and juicy at least in A. elasticus 
Blume and A. sericicarpus Jarrett). In contrast with this comparatively undifferen- 
tiated internal structure the external appearance of these syncarps is remarkably 
varied, depending on the shape and indumentum of the perianth apices. They 
range from scarcely projecting so that the surface appears areolate, each areola 
representing the tip of a perianth, to long drawn-out and flexuous, giving the 
figurative appearance of the head of a Medusa. Such elongation of the perianth 
apices is often associated with dimorphism. There is then usually a marked 
contrast between the short, perforate apices from which the styles emerge and the 
intermingled solid processes, which may bear distinctive hairs — long, appressed 
and silky in A. sericicarpus but short and patent in A. elasticus (Terap in Malaya) and 
recurved in A, tamaran Becc. and A. multifidus Jarrett. In A. teysmannii Miq., on 
the other hand, comparatively few of the perianth apices are elongate and inter- 
mediates occur. It is interesting to note that this dimorphism is found in one or 
more (but not all) of the species in each of the three series in Sect. Artocarpus 
(Incisfolii, Angusticarpi and Rugosi) which have this type of syncarp and that it 
apparently represents parallel evolution. 


The fourth series in this section (Cauliflori) possesses the most remarkable 
syncarps in the genus. The enormous fruits of A. heterophyllus Lam. (Jack) and 
A. integer (Thunb.) Merr. (Chempedak), which are borne on the trunk and larger 
branches, may measure as much as one metre in length and half a metre across. 
The very numerous seeds are enclosed in the strongly hypertrophied proximal free 
region of the perianths and in the Chempedak (but not the Jack) these separate 
from the wall and the core at maturity, falling out when the baggy syncarp is cut 
open. The taste and smell is highly characteristic of each species and was described 
by Corner (1939) as “‘sickly sweet” in the Jack and much stronger (‘‘of durian 
and mango”’) in the cultivated Chempedak (but lacking in the wild var. silvestris 
Corner). The syncarp surface is covered by firm, but not indurated, conical 
perianth apices. 


The smaller, globose or short-cylindric, armoured fruits of sect. Duricarpus 
representing the third type of syncarp in subg. Artocarpus, have seeds that are 
likewise surrounded by succulent, hypertrophied perianths. The free tips of the 
perianths are, however, woody and, while in some species such as A. lanceifolius 
Roxb. (Keledang) and the pinnate-leaved A. anisophyllus Mig. they are merely 
cylindric, in others such as A. rigidus Bl. (Monkey Jack) and the related A. 
hispidus Jarrett, they form tapering spines. 


The smooth or papillate, fleshy syncarps of subg. Pseudojaca (Tampang in 
Malay) present a strong contrast to those just described and, as already stated, 
there is relatively little variation in appearance and morphology. Only in A. 
styracifolius Pierre from southern China is the surface covered by flexuous pro- 
cesses and these appear to be formed from enlarged interfloral bracts. (Bracts are 
present among the flowers in most species of Artocarpus at least in juvenile 
inflorescences but their heads are usually minute and discoid or infundibuliform.) 
As regards internal structure, where the proximal portion of the perianths is free 
it is thin-walled, but in several species, including A. fulvicortex Jarrett among 
Malayan species (Orange-Barked Tampang in Corner, 1940), the perianths are 
completely fused. Finally a few species in subg. Artocarpus such as A. kemando 
Miq. have small fleshy fruits which should be classified biologically with this group. 

The biological significance of the syncarp in Artocarpus was taken up by 
Corner is his discussion of the Durian Theory, in which the genus was frequently 
mentioned (1949, 1954a, 1954b). Vegetatively it shows both massive pachycaul 


38 Gardens’ Bulletin, Singapore — X X1X (1976) 


and slender leptocaul construction and, in particular, the association of the latter 
with cauliflory in A. integer and A. heterophyllus, The compound syncarp, more- 
over, shows striking parallels in some species with fruits of the Durian type. The 
surface may be armoured but here this is by perianth apices rather than by simple 
spines; the fruit may be strong smelling as, for example, in A. elasticus, A. hetero- 
phyllus and A. integer; and; finally, fleshy perianths can take on the function of 
an aril (Corner, 1962). However, other parallels may also be seen in the genus 
since the fleshy syncarp. of subg. Pseudojaca can be compared with a berry, 
although the flesh is formed from the perianths and axis rather than from the 
carpel wall. It may be added that in the allied genus Prainea, in which the 
perianths remain free in the female inflorescence, the few that form seeds and 
project from the surface each resemble a single-seeded berry in which, again, the 
flesh is formed by the perianth. 


It might be assumed that these biological variations in the syncarp would be 
reflected in marked differences in the animals acting as distributors. However, 
while differences do exist they are not verv clear-cut. Precise information is scanty 
and mainly derived from cultivated trees, which is not surprising since in the forest 
Artocarpus is usually widely scattered. However, it is clear from observations 
gathered together by Ridley (1930) and others made by Corner (1939, 1940) that 
it is the attractive flesh, variously dispersed in the syncarp, that brings about the 
distribution of the seeds. Arboreal mammals, especially monkeys and civet cats 
break open the larger fruits, nibbling the juicy perianths and scattering at least 
some of the seeds. Docters van Leeuwen (1935) also records several species 
including two of the most important cultivated species, Chempedak & Breadfruit. 
as being eaten by bats, a fact first mentioned by Rumphius. Ridley suggests that 
the cauliflorous fruits are eaten by wild pig, cattle and elephants. The smaller 
fleshy fruits may be eaten by birds or bats and could be carried off whole and 
thus more widely distributed. However the distribution patterns of the species, 
which were mapped in my monograph, suggest that water is a strong barrier to 
dispersal, as might be expected with such large seeds lacking in dormancy. 


The uniqueness of the syncarp in Artocarpus lies in the partial fusion between 
tubular perianths which exists in most species. This character has made possible 
the differentiation for attractive or protective functions of the proximal and distal 
regions of the perianth and hence the remarkable biological parallels between this 
compound fruit and syncarps derived from a single flower. It is evident that field 
observations are still needed to enrich our biological knowledge of this diverse 
genus. 


REFERENCES 


CORNER, E. J. H. 1939. Notes on the systematy and distribution of Malayan 


phanerogams, IT. The Jack and the Chempedak. Gdns’ Bull., Singapore 10: 
56-81. 


1940. Wayside Trees of Malaya, Vol. 1. Govt. Printer, Singapore. 
770 pp. 


1949. The Durian Theory or the origin of the modern tree. Ann. 
Bot. N.S. 13: 367-414. 


— 1954a. The Durian Theory extended — II. The arillate fruit and 
the compound leaf. Phytomorphology 4: 152-165. 


1954b. The Durian Theory extended — III. Pachycauly and 
megaspermy — Conclusion. Phytomorphology 4: 263-274. 


1962. The classification of Moraceae. Gdns’ Bull., Singapore 19: 
187-252. 


: 


: 


Syncarp of Artocarpus 39 
DOCTERS Van LEEUWEN, W. M. 1935. The dispersal of plants by fruit-eating 
bats. Gdns’ Bull., Singapore 9: 58-63. 


JARRETT, F. M. 1959a. Studies in Artocarpus and allied genera, I. General 
considerations. J. Arnold Arbor. 40: 1-29. 


1959b. Studies in Artocarpus and allied genera, III. A revision of 
Artocarpus subgenus Artocarpus. J. Arnold Arbor. 40: 113-155, 298-368. 


1960. Studies in Artocarpus and allied genera, IV. A revision of 
Artocarpus subgenus Pseudojaca. J. Arnold Arbor. 41: 73-140. 


RIDLEY, H. N. 1930. The Dispersal of Plants Throughout the World. Reeve, 
London. 774 pp. 


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The Origin of the Afroalpine 
Pachycaul Flora 


and its Implications 
by 


D. J. MABBERLEY 
Botany School, Oxford 


Summary 


The morphological, anatomical and biogeographical implications of the apparently 
primitive nature of the forest pachycaul form in Senecio and Lobelia are discussed. The 
preadaptation of high altitude swamp pachycaul forms for temperate rhizomatous vegeta- 
tion and the adaptations of hyperpachycaul forms to the conditions of the tropical alpine 
belt are stressed. 


Fig. 1. Lobelia rhynchopetalum in the High Simien of Ethiopia during von Riippell’s 


expedition of 1833. (From von Riippell, 1840: t. 6 i issi 
University Librarian, Cambridge. a Petr Romer eee ie be olecunn 


perder charakterisert diese Zone eine sehr fremdartige Pflanze, die einer Aloekrone 
oy * welche auf einem mannshohen hohlen Stengel aufsitzt. Ihr Landesname ist Gibarra, 
int systematische Stelle die Familie der Lobeliaceen. Da sie nur an der Schneegranze 


vork6mmt, und doch in der Form eini i it mi i i 
. uae uge Ahnlichkeit mit den der warmsten Tropenvegetation 
eigenthiimlichen Pflanzen hat, so gibt dieses der Landschaft einem hochst fremdartigen 
Charakter. 
Eduard von Riippell (1836). 
4] 


42 Gardens’ Bulletin, Singapore — XX1X (1976) 


Introduction 


With the baobab and Welwitschia, the Giant Groundsels and Lobelias are 
perhaps the most famous botanical curiosities of Africa. The layman’s familiarity 
with herbaceous senecios and lobelias, the unfamiliar habit of the ‘giant’ plants 
and their exotic tropical montane home have given the Giant Groundsels and 
Lobelias an exalted place in botanical travelogues, popular horticultural works and 
other writings and made them a tourist attraction attained by few members of the 
vegetable kingdom. 


The adjective ‘giant’ in botanical works has connotations of teratology or 
polyploidy and is used here only in the nicknames ‘Giant Groundsels’ for Senecio 
L. subg. Dendrosenecio Hedb. and ‘Giant Lobelias’ for Lobelia L. sect. Rhyncho- 
petalum (Fres.) Benth. & Hook.f., the general term ‘“pachycaul’ being used for 
those plants with massive primary construction, large buds and large leaves, of which 
fine examples are provided by the Giant Groundsels and Lobelias (Corner, 1949). 


Pachycaul senecios have been known from Africa since the eighteenth century; 
those first brought back to Britain were not from the continent but from the 
isolated Atlantic island of St. Helena, 900 km east of the Mid-Atlantic Ridge 
(Mabberley, 1975b). Later, pachycaul species were discovered in West Africa and 
Ethiopia where the first pachycaul lobelia was collected (Fig. 1); finally the 
mountains of tropical East and Central Africa were rediscovered and the famous 
Giant Groundsels and more Giant Lobelias collected for the first time, in the latter 
half of the last century. 


Meanwhile the alpine belts of the Andes yielded the pachycaul “‘Frailejones” 
(Espeletia spp.) and puyas, and although pachycaul plants are not restricted to 
islands and mountain-tops (Corner, 1949), their conspicuous appearance in such 
situations, and the superficial correlation between their presence and the ‘insular 
situation’ had aroused considerable discussion. The study of the floras and faunas 
of islands, continental and oceanic, and of insular situations, geological and 
altitudinal, has been of continuous interest to biologists, for much evidence for the 
theory of Natural Selection was derived from it by Darwin, whose observations in 
the Galapagos Islands paved the way to modern ideas on evolution: 


“The principle which determines the general character of the fauna and flora 
of oceanic islands, namely that of the inhabitants, when not identically the 
same, yet are plainly related to the inhabitants of that region whence colonists 
could mostly readily have been derived — is of the widest application 
throughout nature .... For alpine species, excepting in so far as the same 
forms, chiefly of plants, have spread widely throughout the world during the 
glacial epoch, are related to those of the surrounding lowlands.” 


Charles Darwin, Origin of Species (1859: 342) 


The fallacy in the blind comparison of ‘altitudinal islands’ and oceanic islands 
has been explored by White (1971). Nevertheless, certain families, e.g. Campanu- 
laceae and Compositae are represented by pachycaul forms on islands both 
geographical and altitudinal. One genus in each of these families viz. Lobelia and 
Senecio is similarly distributed. Within their respective families, these genera are 
large, Lobelia with perhaps 350 species (Wimmer, 1956, 1968) and Senecio, as 
understood at present, is perhaps the largest of flowering plant genera with 2000- 
3000 species (Willis, 1973). Unlike other genera with arborescent forms in these 
predominantly herbaceous families, Lobelia and Senecio have herbaceous as well 
as woody forms (Good, 1974: 85) and almost the whole gamut of life-forms 
represented in their families is to be found in them. If the genera, or sections of 
them, are monophyletic, then it should be possible to discern evolutionary trends 
within them and hence investigate the relationship of the pachycaul habit to that 


4 
f 
* 


9 


Afroalpine Pachycaul Flora 43 


of the herbaceous habit. It is only in the mountains and on the islands of Africa 
that pachycaul species of both genera grow together. Thus it was felt that a study 
of these ‘Giant Lobelias and Groundsels’ would throw considerable light on the 
evolution of the woody pachycaul in florally advanced families. Currently seven 
pachycaul species of Senecio (Mabberley, 1973a; 1974a; 1975b) and seventeen 
pachycaul species of Lobelia (Mabberley, 1974c) are recognized. Revisions had 
been made piecemeal before those, but the origin of the pachycaul habit was 
undecided through the lack of either developmental studies or the comparison of 
pachycaul with herbaceous forms. In consequence, two opposing theories had been 
proposed. Fries & Fries (1922) suggested that the pachycauls were primitively 
forest plants of the Tropics, whereas Cotton (1944) argued that they had arisen 
from temperate plants which had reached the Tropics along mountain chains and 
elaborated pachycaul construction there. Recently these arguments have been 
voiced by Coe (1967) and Carlquist (1965: 199) respectively. 


Besides in these speculations, the Giant Groundsels and Lobelias appeared in 
a more profound work, the Durian Theory of Corner (1949-54b; 1964), the 
pachycaul construction which they exhibit being a keystone of much of the theory, 
which argues the origin of leptocaul trees from pachycaul ancestors. Are they 
relics of those from which the leptocaul and herbaceous evolved and multiplied 
to populate the temperate zones, or are they rare elaborations of herbaceous groups 
selected for their longevity in ‘insular situations’? 


Senecio 


The first African pachycaul senecios to be discovered were S. leucadendron 
(Forst.f.) Hemsl. and S. redivivus Mabberley, the He—- and She— Cabbage Trees 
respectively, first collected by Banks on St. Helena on Cook’s Endeavour voyage 
in 1771 (Mabberley, 1975b). No pachycaul species from the mainland was collected 
until 1859, when Sir John Kirk collected scraps of a woody Senecio on Living- 
stone’s Zambezi Expedition; his specimens were not received at Kew until 1867, 
by which time the tree had been discovered on Clarence Peak, Fernando Po in April 
1860 by Gustav Mann, whose name it bears, Senecio mannii Hook.f. It is now 
known from Nigeria, Cameroun and from Zaire to Ethiopia and Tanzania, 
Mozambique and Angola (Mabberley, 1973b). In June 1864, the Middle East 
botanist Wilhelm Georg Schimper collected a related species, S. gigas Vatke, on his 
third expedition in Ethiopia. 

It was not until the Royal Society and the British Association put the ‘Kilima- 
Njaro Expedition’ of 1884 into the field with the energetic Harry Hamilton 
Johnston as its leader that the first Giant Groundsel was collected and named 
S. johnstonii Oliv.; later many collections from the other mountains were also 
given specific rank, but with S. johnstonii these are now considered to constitute 
three species in all (Mabberley, 1973a), the second being S. keniodendron R.E. 
& T.C.E. Fr., an hyperpachycaul tree of Mt. Kenya and S. brassica R.E. & T.C.E. 
Fr., a ‘creeping tree’ of Mt. Kenya and the Aberdare Mts. of Kenya. The African 
pachycaul senecios are thus: Senecio leucadendron, S. redivivus, §. mannii, S. 
gigas, S. johnstonii comprising eight geographical and altitudinal subspecies includ- 
ing subsp. refractisquamatus (De Wild.) Mabberley and subsp. barbatipes (Hedb.) 
Mabberley, §. keniodendron and S. brassica. 


In Hoffmann’s treatment of Senecio (1892), all the Giant Groundsels then 
known as well as the Cabbage Trees and S. mannii and S. gigas were included in 
the ‘Arborei’, an heterogeneous assemblage of species put together merely on their 
woody habit; some leptocaul shrubs of Madagascar were also included. Recent 


44 2 Gardens’ Bulletin, Singapore — XX1X (1976) 


study of the details of the flowers (Mabberley, 19742) has shown that the 
allegiance of the Giant Groundsels is with the herbaceous sect. Crociserides, that 
of S. gigas and S. mannii with the lianoid and herbaceous ‘Crassocephalum-Gynura’ 
complex, whilst S, leucadendron is quite isolated in the genus as is S. redivivus. It 
is more easily argued (Mabberley, 1974a) that the tropical pachycauls with the 
primitive ‘Dendrosenecio-branching’ are relics of a pachycaul ancestry for the 
herbaceous group than that they are sporadic arborescent innovations from primarily 
herbaceous stocks. This is supported by the observation that pachycaul trees with 
this branching habit are to be found in other alliances in Senecio in New Zealand, 
Mexico, Cuba and the Canary Islands. 


It was argued that in the Dendrosenecio-Crociserides assemblage, evolutionary 
trends within the Giant Groundsels provided a clue to the origin of the herbaceous 
forms by the stem’s becoming a ‘truncus superficialis’ as in S. brassica and thence 
a subterranean rhizome suited to perennation and the invasion of the temperate 
zones (c.f. ‘herb-making’ in Hedysarum, etc. analyzed by Gatsuk, Dervis-Sokolova, 
Ivanova & Shafranova (1974) ). The massive alpine pachycauls, ‘hyperpachy- 
cauls’, are seen as dead ends as far as evolution of temperate vegetation is con- 
cerned, but adapted to the exacting climate of the afroalpine belt in elaborating 
characters such as leaf-movements etc. (see below). By contrast the creeping form 
adapted to the swampy habitat is seen as pre-adapted to a seasonal climate. 


ALPINE PACHYCAULS 


In the pachycaul alpine species are elaborated certain characteristics which are 
weakly developed in the forest forms. Marcescence is more marked; Hedberg 
(1964) has shown that the marcescent collars of leaves act as efficient insulators, 
the temperature around one tree dropping to —4°C, whilst remaining + 1.8°C 
within the ‘collar’. This warm microhabitat is exploited by animals, e.g. the frills of 
S. keniodendron provide a night shelter for the chironomid midges which breed in 
the buds of Giant Lobelias, and for many beetles and spiders (Coe, 1967) whilst 
the groove-toothed rat, Otomys orestes orestes Thomas burrows up into the 
marcescent leaves and leaf-bases (Coe, 1967). In another tree, Hedberg (1964) 
found that the pith remained at + 3°C whilst the temperature dropped to —5°C 
outside. If the collars are removed, Hedberg suggests that the tree may die. In 
S. johnstonii subsp. barbatipes, an alpine plant of Mt Elgon, the rdle of the frills 
is taken by the highly developed bark, which is again exploited by animals. As 
Dendrosenecios are hygrophilous, they are often to be found in hollows which are 
frost pockets, where insulation is even more important than in the plants of the 
steep slopes. The movements of the leaves which protect the bud (Diels, 1934: 68) 
and the production of antifreeze slime are also exploited by the invertebrate fauna 
which overnight in the ameliorated micro-habitat thus provided, e.g. snails and 
insects which also receive shelter from desiccation by day (Coe, 1967). 


The marked xeromorphy of alpine forms (Hare, 1941) is linked with the 
severe alpine climate; the thick leaves may be important in preventing water loss. 
The pubescence of the leaves of many forms may reflect incoming radiation 
(Hedberg, 1964), but several alpine forms, e.g. S. keniodendron have glabrous 
leaves. The shiny adaxial surface may be of importance in reflection of radiation. 
The abaxial surface of the leaves of S. brassica may protect the bud at night when 
closed over it by preventing outward radiation, as has been discovered by the 
scarlet-tufted malachite sunbird, Nectarinia johnstonii johnstonii Shelley, which 
gathers the hairs to line its nest (Coe, 1967). There is marked endemism in the 
insects paralleled by their host distribution patterns. Further, there is an increase 
in flightlessness with altitude, probably associated with the alpine habitat stadtives 
‘cryptozoic’ modes of life (Salt, 1954). 


Afroalpine Pachycaul Flora 45 


Lobelia 


The first pachycaul Lobelia from Africa was collected by the zoologist, Eduard 
von Riippell, in the High Simien in Ethiopia in 1833 (Fig. 1). Now seventeen (one 
undescribed) such species are known and all are referable to sect. Rhynchopetalum 
(Fres.) Benth. & Hook.f. (Mabberley, 1974c), in subsect. Haynaldianae E. 
Wimmer, subsect. Nicotianifoliae Mabberley and subsect. Rueppellianae Mabberley. 
The Haynaldianae are a Brazilian group with three African outliers. The Nicotiani- 
foliae are found from eastern Africa to S.E. Asia with closely related taxa in 
Hawaii (Mabberley, 1974c). They include L. giberroa Hemsl. of montane forest 
and clearings and L. bambuseti R.E. & T.C.E. Fr. of the upper forest belt. The 
alpine species are the creeping L. deckenii (Asch.) Hemsl. and L. rhynchopetalum 
Hemsl. of the Rueppellianae and, of the Nicotianifoliae, L. wollastonii Bak.f. and 
L. telekii Schweinf., which seem to be parallel alpine types as is L. nubigena Anth. 
of Bhutan in the L. nicotianifolia [Roth ex] R. & S. complex. All seem to be derived 
from forest ancestors (Mabberley 1974c, 1975a). In the Far East the Nicotianifoliae 
include the rhizomatous L. sumatrana Merr. of high mountains. 


ALPINE PACHYCAULS 


The stems of the forest species of Giant Lobelia are usually bare of marcescent 
foliage; the stems of the alpine species are either prostrate, as in the paludal 
L. deckenii, acaulescent as in L. telekii, or erect, with a conspicuous frill of 
marcescent foliage like that of a Dendrosenecio as in L. wollastonii. The base of 
the leaf has a plug of corky tissue which holds the withered lamina to the stem. 
Erect flowering shoots of L. deckenii are also thus clothed as figured by Hedberg 
(1964). Diurnal leaf movements of the leaves also protect the buds which are 
bathed in antifreeze slime as in Senecio. 


Coe (1967) reports that chironomid midges shelter in the closed rosettes of 
Lobelia deckenii subsp. keniensis and that the larvae are found in the slimy water 
therein. The water is said never to dry up, even in cultivation (McDouall, 1927) 
and does not freeze solid except at very low temperatures: the larvae are thus 
protected. Hedberg (1964) measured the temperature outside and inside the bud 
of Lobelia telekii and found it to drop to -3.5°C outside, whilst falling no lower 
than +1.0°C within. 


Scott (1935) worked on the assemblages of Coleoptera restricted to the 
pachycaul lobelias. Some species, e.g. a silphid, spend their entire life cycle in a 
Lobelia plant as do certain bibionid flies in Lobelia flowers (Coe, 1967). The 
distribution of the associated species of Trechus (Coleoptera) matches that of the 
lobelias (Scott, 1958). As with those of the Dendrosenecios, many of the insects are 
flightless and ‘giant’ within their own genera. 


Dendrosenecio, Rhynchopetalum, and Altitudinal Distribution 


The study of the pachycaul Lobelioideae and Senecioneae of Africa has given 
support to Croizat’s (1962: 257) forecast of ‘similar’ evolutionary patterns in the 
Giant Groundsels, Lobelias and the South American espeletias. This study has 
supported the view of the origin of alpine forms from forest ones in parallel as 
eh by Humbert (1935) for Dendrosenecios and Fries & Fries (1922) for 

elia. 


Dendrosenecios occur on the wet mountains of eastern Africa at altitudes 
over 2100 m, but only on those mountains higher than 3300 m. Although found 
on the Cheranganis (c. 3400m), they are not found on the nearby Mau Massif 
(3050m); the difference between these two appears to be critical. Similarly, the 
difference between the Aberdares (3940m) and the Cheranganis may be critical 
for Lobelia telekii, which is absent from the latter range. 


46 Gardens’ Bulletin, Singapore — X X1X (1976) 


Dendrosenecio and Lobelia telekii distributions may be explained by the 
hypothesis of Wood (1971), wherein former amelioration of climate would have 
forced the Senecio and Lobelia belts to higher altitudes; those mountains, which 
were high enough to harbour them then, still possess them, now that the vegetation 
belts are once more depressed. The adaptive radiation of the Dendrosenecios seems 
not to have proceeded as far as that in Lobelia in the East African mountains, It 
may be that the longer life-cycle of the Dendrosenecios has permitted slower change 
(c.f. Arber, 1928). 


Argument 


Starting from the pachycaul members of both genera, interpretations of many 
morphological and ecological features are possible. Can as much be explained if 
herbs are taken as the primitive condition and the pachycaul as the advanced? 


Starting from herbs in the Crassocephalum-Gynura and Crociserides alliances 
of Senecio, it is necessary to postulate a mechanism for increasing woodiness (that 
so far suggested (Carlquist (1962) ) seems to be untenable (Mabberley (1974b) ), 
and for postponing flowering. All the available evidence points to a forest ancestry 
for the creeping swamp pachycauls and the erect alpine ‘hyperpachycauls’ so that 
there would be no indication of how the presumed herbaceous ancestors attained 
the forest pachycaul condition. S$. brassica would be a ‘herb’ for the second time 
in its evolution (c.f. Arber, 1928). It would have to be argued that the characteristic 
‘Dendrosenecio-branching’ (‘Modéle de Leeuwenberg’ of Hallé & Oldeman, 1970) 
had been attained in herbaceous, succulent, woody, lianoid and pachycaul groups 
independently; furthermore, in the wholly pachycaul groups, there would be no 
indication of their presumed herbaceous ancestors. 


Similarly, it must be argued that several herbaceous lines of distinct appearance, 
e.g. in Lobelia, plants like L. sumatrana and L. deckenii, have colonized the 
Tropics and produced very similar pachycaul plants in America and Africa as well 
as India and Hawaii. It must also be assumed that the inflorescence has become 
more complicated, the fruit baccate, the seeds winged and the leaf-size increased, 
all in several lines. If this is so, then wind-pollination and dispersal must be 
antecedent to bird and insect pollination and dispersal, the short-lived temperate 
herb antecedent to the tropical pachycaul (c.f. Mabberley 1975a). 


No sense can be made of phytogeography, associations with animals or the 
origin of a range of life form within plant genera. It is simpler, then, to follow the 
easier line of argument, and, in short, arrive at the same conclusion as Corner 
(1967b) working with the woody genus Ficus, for if the herb (Senecio, Lobelia) 
or leptocaul tree (Ficus) is primitive and the pachycaul advanced, then: 


(i) The primitive species are the most common and widespread, contrary to 
much of biogeography which would have the primitive as relics; 


(ii) the pachycauls are advanced but make least contribution to tropical forest 
(Ficus) or temperate floras (Senecio, Lobelia) which the flowering plants have 
been evolving; 


(iii) the most leptocaul trees (Ficus) or herbs (Senecio, Lobelia) have the 
simplest inflorescences, supplying no evidence of their evolution. 


As Corner continues, morphological series, [whether i in Ficus, the Crociserides, 
‘Crassocephalum’ or Rhynchopetalum] can be read in either direction; the ecologi- 
cal factor is ‘time’s arrow’. In the case of Ficus, the arrow is aimed at tropical 
rainforest via leptocaul trees; in the Crociserides it is aimed at the conquest of the 
temperate zones via preadapted rhizomatous perennials, in ‘Crassocephalum’ at 
filling the secondary habitats of the African Tropics with fast-growing plants and 
in Rhynchopetalum it is aimed at both. 


Afroalpine Pachycaul Flora 47 


The hypothesis 


The hypothesis is that Lobelia sect. Rhynchopetalum and Senecio sect. 
Crociserides are derived from pachycaul ancestors and that, in parallel, these groups 
have given rise to herbs which have reached the temperate zones, and to 
extreme ‘hyperpachycaul’ forms which have conquered the tropical mountains 
of Africa, living in wet situations above the treeline away from other arborescent 
competition. The hypothesis implies that there have been physiological and 
morphological adaptations for simplification and overwintering in the herbs and 
remarkable elaborations of characteristics of the forest plants in the hyperpachy- 
cauls adapted to the alpine environment. 


The evolution of subg. Dendrosenecio and sect. Rhynchopetalum in Africa 
can be seen as the conquest of the highlands, either by becoming hyperpachycaul 
with marcescent foliage, reduction of hydathodes, enhanced pubescence, etc., or by 
becoming prostrate and lying down in wet places. The latter is the method which 
has permitted the colonization of the temperate zones in these groups. The marked 
increase in pachycauly with altitude may have an ecological explanation, for 
Daubenmire (1947: 186) has shown that massive organs may withstand short 
periods of extreme temperatures better than less massive ones. Hyperpachycauls 
are thus adapted to diurnal climate fluctuations, whereas rhizomatous plants with 
intermittent growth are adapted to a seasonal climate. It becomes clear then, why 
no Lobelia of North Africa and the Mediterranean is of the Rhynchopetalum 
alliance compared with the Crociserides with many Asian and European relatives, 
for, in Africa, the alpine species which reaches furthest north is the hyperpachycaul 
L. rhynchopetalum with a highly peculiar structure; herbaceous Rhynchopetala are 
the result of ‘miniaturisation’ (Hallé & Oldeman, 1970: 150) in the Far East. 


On the other hand, sect. Rhynchopetalum has reached the Pacific as fast- 
growing pachycauls from both east and west, such that the presence of pachycauls 
on both sides of the Pacific is readily explicable (Mabberley, 1975a). Indeed, the 
immigration of the ‘pachycaul starter’ has permitted the development of herbaceous 
plants from Japan to Sumatra. By contrast the Crociserides seem to have spread 
very little as pachycauls but have romped and excelled in the temperate zones as 
coarse herbs. 


Sect. Rhynchopetalum and ‘Crassocephalum’ have elaborated fast-growing 
pachycauls, which have thus become ‘nomads’ (van Steenis, 1958) of the sub- 
montane forests of Africa, and India, incidentally predisposing them to cultivation 
as shamba [small-holding] hedges (S. mannii) (Mabberley, 1974a) and as pot 
plants (L. nicotianifolia [Roth ex] R. & S. (Anon., 1904) etc.) in Victorian green- 
houses. By contrast, subg. Dendrosenecio with a longer life-cycle has ascended the 
mountains to make woodlands above the ‘treeline’. 


In general, then, there is factual support for the predictions of the Durian 
Theory, with the important proviso that the groups here studied are capable of 
hyperpachycauly under the selective pressure of the alpine environment. 


Implications 

According to our hypothesis, then, such statements as “... highly probable 
that the development of the arborescent habit and delayed flowering among the 
tree Senecios and Lobelias of the East African Mountains, was a photoperiodic 
response ... fixed by Natural Selection”, (Melville, 1953) and “‘The ancestors of 
the equatorial alpine rosette trees are temperate zone herbs, which arrived on the 
equatorial peaks by long distance dispersal just as did the ancestors of island 
rosette trees” (Carlquist, 1965: 200) seem to be unsubstantiated by the available 
evidence. On the contrary, it is more easily argued that the pachycaul state is the 
primitive, which leads to the following considerations. 


48 Gardens’ Bulletin, Singapore — X XIX (1976) 


GROWTH HABIT 
Herbs 


The primitive growth-form in the Senecioneae appears to be Dendrosenecio 
branching, examples of which are found scattered throughout the tribe; it appears 
that it represents the ‘pachycaul starter’ condition for ‘Senecio’. The aerial parts 
of the Crociserides, so difficult to describe in ‘cauline’ terms appear to be inflores- 
cences and are more readily comparable with one another and other life-forms 
once this is recognized. Similarly, the creeping lobelias like L. sumatrana show that 
the aerial parts of many lobelias are also merely ‘inflorescence’. 


Hyper pachycauly 

Enhanced pachycauly exemplified in the alpine hyperpachycauls is a feature 
of both genera. It appears to be associated with the basally growing leaves in these 
families. Thus, under the selective forces of the alpine environment, there are 
hyperpachycaul Dendrosenecios and lobelias in Africa, Pachypodium in the 
Malagasy Mts. (Koechlin, 1969), espeletias in the Andes (Smith & Koch, 1935), 
Saussurea gossipiphora D. Don and Rheum nobile Hook.f. & Thom. in the 
Himalaya (Anthony, 1936) and, under the selective forces of the horticulturalist, 
the hyperpachycaul vegetables such as lettuce and cabbage, large European and 
Asiatic varieties of which are figured by Herklots (1972: 190-224). 


The pachycaul construction of massive buds permits the tolerance of the 
Tageszeitenklima (Troll, 1947) of the tropical alpine belts by ‘arborescent’ plants 
above the tree-line, e.g. besides Senecio and Lobelia in Africa, Puya ramondii 
Harms and Lupinus weberbaueri Ulbr. in the Peruvian Andes (Pontecorvo, 1972), 
Lupinus alopecuroides Desr. (Heilborn, 1925), puyas and espeletias in the 
Colombian Andes (Fosberg, 1944) as well as the Andine Ceroxylon (Corner, 
1966: 289) and even Cyathea in the Papuan mountains (Wardle, 1971), but not 
their spread beyond the Tropics into a seasonal climate. Such diurnal fluctuations 
in deserts may favour pachycauly e.g. Cactaceae, succulent Euphorbia species, 
Yucca spp. etc., and fire may favour pachycaul forms with wide cortex and hence 
deeply seated or weakly developed cambium, e.g. Xanthorrhoea spp. in Australia, 
Aloe capitata Bak. var cipolinicola H. Perr. in the ‘prairies’ of Madagascar and 
again Cyathea in New Zealand and New Guinea. In the dicotyledonous examples 
there is a reduction in branching, and in Puya, the inflorescence is unbranched in 
P. ramondii. Similar simplification of structure is to be found in Echium (Bram- 
well, 1972a). In that genus, and other ‘temperate’ genera, the pachycauls of the 
Canary Islands appear to represent relics of the pachycaul starters which initiated 
the herbaceous lines so common in Europe, e.g. Echium (Meusel, 1952; Bramwell, 
1972a), Sonchus (Bramwell, 1972b), Carlina (Meusel, 1952). Similarly, species 
of Erysimum, Crambe, Aeonium, Chrysanthemum, Campanula, Bupleurum, 
Dendriopoterium, Bencomia, Digitalis and Limonium (‘Statice’) appear as pachy- 
caul relics in the Atlantic Islands (Meusel, 1952). 


STEM ANATOMY 


In general, the anatomy of the herbs in Senecio and Lobelia is a good deal 
simpler than that of their pachycaul relatives — fewer cell-layers, leaf-traces, ducts, 
less modification in the pith and cortex with aerenchyma etc. The seedlings of the 
pachycauls are more ‘conventional’; the differences arise when the apex increases 
in size. 


Cortical and medullary bundles 


Associated with hyperpachycauly, there is the appearance of the phyllodic 
leaf-base and cortical bundles in Lobelia; some species have relic medullary 
bundles showing that the medullary bundle condition is the primitive one in 


Afroalpine Pachycaul Flora 49 


Lobelia, and the cortical bundle condition the advanced. Davis (1961) points out 
that in the Compositae, medullary bundles are particularly abundant in the 
Cichorieae, especially in those plants with the ‘rosette-habit’. 


In Lobelia, the medullary bundles serve the base of the primitive ‘forest leaf’; 
the cortical bundles are often associated with the phyllodic leaf. In a similar way, 
cortical bundles are often associated with leaves of the ‘monocotyledonous’ type 
in the Dicotyledons, e.g. Eryngium spp. of the monocotyledonous habit (Metcalfe 
& Chalk, 1950: 717), Gentianaceae-Gentianoideae (ibid.: 933) and groups with 
leaves which have few costae, e.g. Melastomataceae (ibid.: 637). 


The appearance of cortical bundles seems to be a ‘way out’ in evolutionary 
lines where a larger leaf is being favoured and yet the number of traces to serve 
such a leaf has been lost; hence in Lobelia, the cortical bundles are found in the 
most massive pachycauls (Rueppellianae), whose massiveness has been selected 
for by the alpine and swamp environments. Such bundles also give support to those 
massive inflorescences formed by the reduction of branching of a forest form, and 
for which the capacity for supporting lignification has been lost. 


It has recently been suggested (Zimmermann & Tomlinson, 1972) that the 
regular dicotyledonous ring of vascular bundles may be the equivalent of the outer 
of the monocotyledonous systems seen in some woody monocotyledons. If this is 
indeed the case, then Lobelia sect. Rhynchopetalum may demonstrate how the two 
systems as exemplified by L. giberroa may give rise to the typical dicotyledonous 
system as seen in L. bambuseti by loss of the inner system and the origin of a 
‘monocotyledonous’ system as shown by L. rhynchopetalum with the appearance 
of a ‘new’ cortical system associated with basally growing leaves (c.f. Burtt, 1974). 


Hyper pachycauly 

Selection has favoured the hyperpachycaul in the extreme alpine climate; the 
hyperpachycaul is marked by its massive apex and reduced branches compared 
with its forest relatives. Dominance of the apex over lateral meristems is found 
in the absence of suckers in L. wollastonii, the unbranched inflorescences of the 
alpine L. rhynchopetalum, L. wollastonii, etc. with the basipetal inflorescence 
gradient (Mabberley, 1975a) lost etc., the untoothed leaves of alpine Nicotiani- 
foliae and the large capitula on weakly branched inflorescences of the alpine 
Dendrosenecios; in short, there is a common constraint determining the morpho- 
logy of the hyperpachycaul ‘syndrome’ (c.f. Beketoff, 1858; Uittien, 1928; and 
the particular case of Sonchus (Bramwell, 1972b) ). The balance of growth factors 
determining differentiation in the tissues must be tipped in favour of apical 
dominance. Such may be an increase in ‘auxin’ as has been suggested by Cotton 
(1944) and was discovered in Aster by Delisle (1937) who found that there was 
more auxin in the apices of the inflorescences of A. novae-angliae L. than in those 
of A. multiflorus Ait. which is much more branched, (c.f. also Smith, 1967). 


LEAF 
Venation 


The venation of Senecio (Mabberley, 1973a) and Lobelia (Mabberley 1974c) 
leaves is mainly or entirely basipetally formed. In Dendrosenecio, the fraction of 
the leaf formed acropetally is very small; some herbaceous species have a larger 
part of the lamina thus formed and may be amphipetal. 


In the East African Lobelias, my studies have shown a series demonstrating 
the loss of teeth and acropetally formed venation. This series is interpreted as the 
failing of the marginal meristem in the leaf with the consequent loss of teeth, and 
the increasing importance of the spreading growth of the ‘midrib’, giving the 
phyllodic leaf-base. The reduction of toothing in both Senecio and Lobelia reduces 
the number of hydathodes per leaf. The action of hydathodes is not well understood; 


50 Gardens’ Bulletin, Singapore — X X1X (1976) 


despite their supposed efficiency in extruding water, the hydathodes of the toothed 
leaves of L. assurgens L., a pachycaul of Jamaica, investigated by Shreve (1914) 
could not prevent the ‘injection’ of the leaves by water during heavy rain. 


The reduction of the acropetal venation would appear to be irreversible. 
Vassal (1970) has shown the appearance of the phyllodic leaf in Acacia to be 
polyphyletic and formed in various ways, but that there is a progressive loss of 
pinnae, with a ‘mucro’ left in some species, as in Senecio and Lobelia. 


On the other hand, there appears to be a constraint on the number of primary 
costae derived from basipetal development of the lamina. In Senecio, the largest 
leaves have about 18-20 veins in Dendrosenecio; most herbaceous species have 
costal numbers lower than 18. However, some coarse herbaceous species of Uruguay, 
e.g. S. bonariensis Hook. & Arn., appear to have very large numbers of costae; on 
close examination, it can be seen that the intercostals have been ‘pulled out’ during 
development, thus increasing the apparent costal number, as in S. keniodendron, 
(Mabberley, 1973a). 


Abscission 


Abscission is not a common characteristic in the Compositae (Bentham, 
1873), and is almost restricted to those shrubby and arborescent plants of leptocaul 
construction with narrow leaf-bases, e.g. Brachylaena, These characters tend to be 
associated with the discrete midrib and looped costae, early-formed venation 
consummate with compact buds and the sudden expansion of intermittent growth, 
making them comparable with other tree leaves. The insulating marcescent frills 
and persistent leaf-bases of Dendrosenecio and Lobelia wollastonii are conspicuous 
in the afro-alpine flora. When young, however, al! Dendrosenecios and Lobelia sect. 
Rhynchopetalum display this phenomenon, as do herbaceous species, e.g. L. urens 
L., where the rootstock is covered with persistent leaf-bases (Brightmore, 1968). 


How widespread is the absence of abscission and the persistence of leaf-bases? 
Within Senecio, all herbs examined have persistent leaves and it appears very com- 
monly in the herbaceous Compositae but is more familiar to flower arrangers than 
to monographers. The shrubby S. hypargyraeus DC. (Madagascar), the climbing 
S. maranguensis O, Hoffmann (Tanzania) and the leaf-succulent species are 
exceptions. Their small-based leaves are easily lost, even during drying in the press. 
In the shrubby Compositae, leaf-fall is often not clear-cut and the marcescent 
foliage makes a useful: character for recognizing sterile Compositae in ‘the bush’. 
The leptocaul Brachylaena loses leaves as others are formed (Humbert, 1962: 45) 
or may lose them altogether in the cold season (Lecomte, 1922). However, 
marcescence is a general feature of herbs and pachycauls of Compositae, e.g. the 
pachycaul Espeletia in the Andes and pachycaul Conyza vernonioides (A. Rich.) 
Wild of East Africa. Such persistent leaf-bases cover the ‘stock’ of many herbs, 
e.g. Andryala spp. and Senecio asperulus DC. (Hutchinson, 1946: 255), and make 
the climbing hooks of Mikaniopsis (Exell, 1956). Comparable contrast of leptocaul 
and pachycaul and herb is to be found in the Boraginaceae (s./.) with pachycauls, 
e.g. Echium spp. of the Canary Islands, and herbs, e.g. Myosotis, with marked 
SEEN. compared with the leaf-dropping trees, Cordia and Ehretia, of the 

ropics. 


Much has been written of the ‘abscission layer’ with regard to marcescence, 
but Gawadi & Avery (1950) pointed out that abscission is not always associated 
with such a layer and that the layer is a protective feature of the cicatrice; indeed, 
it sometimes appears after abscission. Nevertheless, the range of forms of marces- 
cence and abscission in monophyletic groups shows that abscission has been gained 
or lost many times in the angiosperms. 


Afroalpine Pachycaul Flora 51 


Many young tropical trees retain their leaves in the dry season (Schaffalitzky 
de Muckadell, 1959) rather like the beech (Knight, 1795) in winter or when kept 
horticulturally short as a hedge. It is one of a syndrome of ‘juvenile’ characters 
(Schaffalitzky de Muckadell, 1959) which appear to represent a primitive condition 
in wood anatomy etc. (Mabberley, 1974 a-b). 


If it is postulated that the primitive pachycaul had marcescent leaves, it seems 
reasonable to argue that such marcescence may have been selected against with 
the increasing trunk size due to increasing wood formation through secondary 
thickening, but elaborated where such a mantle would act as an insulator, e.g. in 
hot conditions the Joshua Tree (Yucca brevifolia Engl.) of the deserts of S.W. 
United States (Menninger, 1967: 2) and in the cold, Espeletia in the Andes. The 
origin of the leptocaul tree in many lines according to the Durian Theory must 
have been accompanied by the origin of the small leaf with abscission which seems 
to have been achieved in various ways (Gawadi & Avery, 1950); especially 
efficient abscission mechanisms would have been selected for in seasonal conditions, 
such as ‘savanna’ and the temperate zones. 


EUROPEAN FLORA 


The ecological preference of lobelias for wet places (Woodhead, 195la) is a 
direct result of a wet tropical ancestry through upland swamp habitats to the 
temperate zones; the predominance of aerenchyma and hydathodes in Lobelia is 
thus explicable as is the remarkable habit of the aquatic L. dortmanna L. The 
rare branching of L. dortmanna inflorescences (Woodhead, 1951b) is explicable 
as an ancestral trait, and the minute undeveloped flowers at the apex and smaller 
cell-size in the upper leaves (Tenopyr, 1918) are to be expected from the primitive 
‘die-away growth’ (Corner, 1949) of the primitive tropical pachycaul ancestor. 


Pachycaul Outlook 


We need to know more of pachycaul plants (Corner, 1967a). In the Com- 
positae, we want to know how some tribes have elaborated leptocaul trees as in 
Dicoma and Brachylaena; the latter genus has even reached the ‘willow pattern 
stage’ (Corner, 1964: 143), the ultimate in leptocauly, in B. neriifolia R.Br. 
(Hutchinson, 1964: 228). Such pachycaul-leptocaul trends are not open to simple 
computer analysis, for they are in parallel within related phylads. Are the principles 
governing pachycauly in Compositae and Campanulaceae of general application? 


In Compositae, we need to know more of hyperpachycauly and _ the 
reappearance of the big leaf when the acropetal venation has been lost, as in the 
lettuce in cultivation, and why the basipetal venation of Compositae never seems to 
exceed about eighteen major costal pairs. We need to know more of the pachycaul 
Dendrocacalia of the Bonin Islands (Tuyama, 1936) and of the Siberian Petasites 
the petioles of which are higher than a man (Gilbert-Carter, 1947: 143). We need 
to know more but we are almost too late: introductions of continental plants to the 
islands of Hawaii and St. Helena, and the introduction of animals to those islands 
and to Kerguelen have had disastrous effects on the passive native pachycauls, In 
the mountains, the puyas are being grubbed up by shepherds, for lambs can get 
entangled in Puya spines (Pontecorvo, 1972) and in Africa, the Dendrosenecios 
of Kilimanjaro are becoming rare through excessive cutting (Hedberg, 1969). 
Having fled the rising forests of leptocauly to reach the refuge of islands and 
mountain, the pachycauls are now cornered by Man the Explorer and Exploiter. 
We scarcely have time to begin to follow the leads to an understanding of plant 
evolution provided by the Durian Theory. 


52 Gardens’ Bulletin, Singapore — XX1X (1976) 


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The Underground Forests of Africa: 


a preliminary review 
by 
FRANK WHITE 


Departments of Botany & Forestry, University of Oxford 


“Evolution in Ficus is from the thick to the thin’ — E. J. H. Corner in litt. 27. ii. 74. 
‘Evolution in Barotseland is from the thin to the thin’. Abbridged summary of this paper. 


Summary 


The growth-form of the geoxylic suffrutex, which has massive, woody, underground 
axes but only annual or short-lived shoots above ground is described. The species considered 
are all related to large forest or woodland trees or lianes and occur in genera with no 
herbaceous members. They are confined to tropical and subtropical savanna regions. Their 
distribution and ecology are considered. Geoxylic suffrutices are most diversified in Africa, 
where they have independently evolved in 31 families. Very few occur in the Sudanian 
Region and they are rare there. Most are endemic to the climatically similar Zambezian 
Region where they are centred on the Kalahari Sands which cover much of the upper 
Zambezi basin and its periphery. Arguments are developed which suggest that the growth 
form of the geoxylic suffrutex has evolved, not primarily in response to fire, nor to frost, 
as has been previously supposed, but as a response to the unfavourable edaphic conditions 
provided by extremely oligotrophic, seasonally waterlogged sandy soils in a region of 
extremely low relief. 


Introduction 


Corner’s fruitful hypothesis, that the proto-Angiosperm was of pachycaul 
construction with an unbranched or sparsely branched stem, monopodial growth, 
massive apical meristem, wide pith and cortex, sparse secondary xylem, very short 
internodes and large compound leaves, illuminates the early adaptive radiation of 
the vegetative architecture of the Angiosperms and has inspired a number of 
important detailed studies (e.g. Hallé & Oldeman, 1970; Mabberley, 1974 a, b). 


The further diversification of the leptocaul descendants of pachycaul plants, 
however, has received much less consideration. The purpose of this short account 
is to draw attention to a group of geoxylic suffrutices, which, despite their short 
stature and quasi-herbaceous habit are closely related to large forest or woodland 
trees or lianes, and, despite their exiguous subaerial parts, usually have massive 
woody subterranean structures. Most of them are trees which, for some reason, 
now live underground. It is interesting to enquire how this has come about. 


Geoxylic suffrutices with this kind of phylogenetic relationship to large woody 
plants are almost confined to those parts of the tropics with a markedly seasonal 
distribution of rainfall, and where the prevalent vegetation is ‘savanna’ in which 
woody plants and grasses occur together in various proportions. The term savanna 
is used here in the general sense of Chapman & White (1970: 82) and not as a 
precise classificatory unit. Today savanna vegetation is everywhere subjected to 
extensive man-made fires and consists largely of pyrophytic species. It has probably 
always been subjected to natural fires which were formerly less frequent and more 
localized. Some authors, e.g. Exell & Stace (1972), believe that the suffruticose 


57 


58 Gardens’ Bulletin, Singapore — XX1X (1976) 


habit in savanna regions has evolved largely as a response to fire. Fire has 
certainly played a part in the evolution of the geoxylic suffruticose habit, but its 
relative importance and significance seem to have been misunderstood. 

The distribution of geoxylic suffrutices within the savanna regions of the world 
is very uneven. Their greatest concentration is in south-central Africa on the 
Kalahari Sands which cover most of the Upper Zambezi basin and its periphery. 
Since other elements in the Zambezian flora also show a similar distribution, White 
(1965) recognized a Barotse centre of endemism, which takes its name from the 
ancient Kingdom of Barotseland, situated near its heart. 


Within the Barotse centre the most characteristic habitat of these suffrutices 
is a sparse open grassland which burns much less fiercely than most savanna vege- 
tation. They are scarce or absent from the more fiercely burning types. This fact, 
and their localized distribution within the fireprone savanna regions, suggests that 
their origin should be sought not exclusively in relation to fire but that other factors 
should be considered. 


A few suffrutices, which occur on Kalahari Sand, also extend their range into 
the Highveld grassland of the Transvaal, and a few others are endemic there. This 
is a part of Africa where frost is severe, a fact which led Burtt Davy, writing at a 
time (1922) when the flora of Barotseland was completely unknown, to suggest 
that the suffruticose habit had been moulded in response to frost. 


For the majority of suffruticose species occurring in the Zambezian Region 
Speciation appears to be complete. Either their geographical ranges overlap with 
those of closely related large woody species, with which they presumably share a 
common ancestor, or they are taxonomically isolated and have no very close 
relatives. For a significant minority, however, speciation is incomplete. Within a 
single species some populations are suffruticose, whilst others are trees, shrubs or 
lianes. By studying these species, together with non-suffruticose species in the same 
general area, which have proceeded part-way towards the suffruticose habit, or 
show, perhaps sporadically, some of the attributes suffrutices must acquire, it is 
possible to reconstruct the probable ancestry of this particular growth form. 


Evidence is presented in this paper which suggests that, in Africa, the geoxylic 
suffrutex originated primarily as a response to extremely unfavourable edaphic 
conditions, but that for some species, at least occasionally, fire is necessary for 
vigorous growth. The suffrutex is better adapted to frost than the tropical trees and 
lianes which gave rise to it, but it is unlikely that frost played any significant part 
in the evolution of the habit. 


Literature on geoxylic suffrutices is sparse and scattered. Only Burtt Davy 
(1922) has attempted a general review. 


Growth Forms 


There are many kinds of suffrutex and the term is often loosely or erroneously 
applied. The stems of a suffrutex are woody at the base and persist for several 
years, giving rise to less persistent shoots, which die back after a relatively short 
time, sometimes each year, sometimes after a longer interval. The suffrutices dealt 
with here are unusual, in that, at least under present-day conditions, their stems are 
burnt back almost to ground-level nearly every year. Suffrutices are clearly adapted 
to this condition. Shortly after burning and well before the onset of the rainy 
season they send out new shoots, which often produce flowers precociously at the 
base of the shoot before it is fully developed. The associated grasses and other 
herbs, which when fully grown may completely conceal the suffrutices, do not 
begin their vegetative development until after the rains break, by which time the 
suffrutices have finished flowering. 


Underground Forests of Africa 59 


The suffrutices dealt with here are very sensitive to fire. Even if their shoots 
are only lightly singed, they die back to the base. A severe fire might kill all the 
subaerial parts, in which case renewal is from subterranean stems and the plant 
behaves as a geophyte. Normally, however, the basal parts of the subaerial stems 
remain and the plant behaves as a chamaephyte. 


Different species of suffrutex, and sometimes different populations within species, 
behave differently when they are protected from fire. In some species there is a 
considerable die-back every year almost to the base. In other species there is a 
limited amount of upward growth which may continue for a few years. In obligate 
suffrutices, however, upward growth is severely restricted and ultimately the 
subaerial parts become moribund. Few flowers are produced and there is pro- 
gressive die-back towards the base. In Parinari capensis all herbarium specimens 
from the northern Transvaal are less than 15 cm. tall. Burtt Davy transplanted P. 
capensis “‘to more favourable conditions of temperature and soil moisture’’ but it 
““did not show any change of habit after several years’. North of the Limpopo, 
when individuals escape fire, they are capable of attaining a height of 40 cm. but 
no more. At the extreme south-eastern limits of its range in southern Mocambique 
and northern Natal it can grow up to a height of 2 m. 


All the suffrutices dealt with here have massive woody underground parts and 
the term ‘geoxylic’, used by Du Rietz (1921) in a somewhat different context, is 
appropriate. In the majority, several axes radiate just beneath the surface of the 
soil from the main vertical subterranean axis, which, except in young plants, is 
relatively poorly developed. Sometimes they extend for a distance of several metres. 
In some species these axes can reach a diameter of 10 cm. or more. They are 
usually very hard and consist mostly of secondary xylem, the total amount of which 
is probably no less than that of a medium-sized woodland tree growing in the same 
general region. These radiating axes are usually referred to as ‘rhizomes’. Their 
true nature, however, requires careful investigation since the arboreal relatives of 
some suffrutices are said to sucker freely from their extensive superficial roots. The 
suffruticose Parinari capensis, for instance, looks very similar to a suckering clump 
of the tree species P. curatellifolia Planch. ex Benth. though their proportions are 
different. 


Some species, e.g. Erythrina baumii Harms, have specialised water-storing tissue 
(Duvigneaud, 1954), but this does not seem to be a general feature. 


Some species are not rhizomatous or only slightly so and the underground part 
consists of a large vertical axis which may be greatly expanded at ground level 
where many annual shoots arise. Rawitscher & Rachid (1946) describe these for 
Cochlospermum insigne St. Hil. and a palm, of the genus Acanthococos. They call 
them ‘xylopodia’ and say they are stems. This type seems to be rare in Africa. 


This account is confined to suffrutices which not only are closely related to 
large trees or lianes and have presumably evolved from large trees or lianes, but 
Occur in genera which except for their suffruticose members consist exclusively of 
large woody plants. Suffrutices of similar habit, though usually with smaller under- 
ground parts, which belong to otherwise shrubby groups are excluded from con- 
sideration. Similarly the suffruticose species of genera which include true herbs and 
trees, e.g. Cassia and Phyllanthus are omitted. 


Fig. 1 illustrates Euclea crispa a typical “‘rhizomatous” geoxylic suffrutex. In 
this polytypic species some subspecies, like the one illustrated are obligate suffruti- 
ces, whereas others are always trees. The latter sometimes occur as single-stemmed 
individuals, but sometimes form thickets of trees which arise from suckers from the 
superficial ‘roots’. 


60 


Gardens’ Bulletin, Singapore — X XIX (1976) 


Fig. 1. Euclea crispa (Thunb.) 
Giirke. A typical rhi 
geoxylic suffrutex. Note the cha 
remains of last-year’s stems. 


Underground Forests of Africa 61 


Distribution and Ecology 


General distribution 

Geoxylic suffrutices are a conspicuous feature of the campos cerrados of the 
Planalto of Central Brazil, and are recorded in the classical literature (Schimper, 
1898: 376; Warming, 1892). No general review has been published but information 
can be gleaned from a scattered literature — Andira inermis Mart. and Anacardium 
pumilum St. Hil. (Rawitscher et al, 1963) Jacaranda decurrens Cham., Cochlo- 
spermum insigne St. Hil. and Acanthococos sp. (Rawitscher & Rachid, 1946), 
Byrsonima verbascifolia Rich. ex Juss. (Aubréville, 1961), Chrysophyllum soboli- 
ferum Rizzini (Mangenot, 1969), Licania dealbata Hook. f. and Parinari obtusifolia 
Hook. f. (Prance, 1972), and Caryocar brasiliense Cambess. subsp. intermedium 
(Wittmack) Prance & Freitas da Silva (Prance & Freitas da Silva, 1973). 

It appears that geoxylic suffrutices are fewer in species in South America than 
in tropical Africa, and that taxonomically isolated, obligate suffrutices are pro- 
portionally less well represented. 

In Asia it appears that there are very few geoxylic suffrutices. From Australia 
they seem to be absent, though many multiple-stemmed, tall-shrubby species of 
Eucalyptus have large woody underground parts (mallee). 


It is in tropical Africa that this growth form is found in its greatest diversity. 
Here there are no less than 109 species belonging to 56 genera occurring in 31 
families. These are listed systematically in an appendix. 


Distribution in Africa 

In Africa geoxylic suffrutices are almost confined to the two great savanna 
regions — the Zambezian and Sudanian. Only a few species occur in the transitional 
region to the south of the Zambezian Region, the prevalent vegetation of which is 
grassland and wooded grassland. There are also a few others in the southern part 
of the Indian Ocean coastal belt, the Tongaland-Pondoland Region, which is a 
mosaic of savanna-like and forest formations (Fig. 2). Since very few species are 
confined to the Tongaland-Pondoland Region it is not considered further. 


The Sudanian Region occurs as a wide band north of the equator between the 
rainforests of the Guineo-Congolian Region and arid and semi-arid regions to the 
north. The Zambezian Region occupies a comparable position south of the equator. 
In area these two regions are comparable. Their vegetation which consists mainly 
of woodland, wooded grassland and various types of edaphic and secondary 
grassland, is broadly similar, as is their climate. The mean annual rainfall varies 
from 500 to 1500 mm. and the dry season lasts from 5 — 7 months. The Zambezian 
Region, however, is somewhat more diverse in its physiography and climate. In 
both regions dry season fires are an annual occurrence over extensive areas. Neither 
region can be said to be more fire-prone than the other. 


The representation of geoxylic suffrutices in the two great savanna regions is 
very uneven. Only 7 species belonging to 2 genera in 2 families are known from 
the Sudanian Region, whereas 102 species in 55 genera in 30 families occur in the 
Zambezian Region. Of the 7 Sudanian suffrutex species, 6 belong to the genus 
Combretum and 5 of them are closely related. 4 species are of very restricted 
distribution and are confined to upland areas such as Fouta Djallon and the Jos 
Plateau. Another species, C. sericeum G. Don f., is of uncertain taxonomic status and 
is connected by intermediates to a climbing species, C. paniculatum Vent. 


The Sudanian and Zambezian Regions are so different in their suffruticose 
floras that an explanation must be sought, either in their unequal opportunities for 
the evolution of suffruticose species or in those for the survival of a suffruticose 
flora which was formerly common to both. 


62 Gardens’ Bulletin, Singapore — XX1X (1976) 


It is well known that the flora of the Sudanian Region is, in general, much 
poorer than that of the Zambezian Region. In two analyses of the larger woody 
plants occurring in the two regions, White (1962, 1965) has shown that the flora 
of the Zambezian Region is probably between two and four times as rich as that 
of the Sudanian Region. He suggests (1962) that this may, at least in part, be due 
to differential extinction during the Pleistocene. A region as physiographically 
diverse as the Zambezian offers better opportunities for migration and survival 
than does a region of low general relief such as the Sudanian. There is much 
phytogeographical evidence to support this idea. Several species which are wide- 
spread in the Zambezian Region, e.g. Ochna schweinfurthiana F. Hoffm., Protea 


a 
FROMONTE 


OG 
ees 
bes 


Fig. 2. Map of Africa showing chorological regions referred to in the text. 


Underground Forests of Africa 63 


madiensis Oliv., Terminalia mollis Laws., are very sporadic in the Sudanian Region. 
Their distributions suggest that in the Sudanian Region they have only just avoided 
extinction due to climatic change. If they have only just managed to persist, is it 
not likely that some of their former associates have perished? Similar considerations 
might apply to the suffrutices, but here the discrepancy between the two regions is so 
much greater — the Zambezian suffruticose flora is 15 times as rich as the 
Sudanian and, at the generic level, 22 times as diversified — that the explanation 
must surely be sought in differential opportunity for speciation. This leads us to a 
consideration of the ecology of geoxylic suffrutices. 


Ecology in Africa 


The most characteristic habitat of the geoxylic suffrutex in the Zambezian 
Region is seasonally anaerobic grassland, mostly on sandy, extremely oligotrophic 
soils, which are waterlogged and badly aerated for part of the year and dry out at 
least in their upper layers during the dry season. Such conditions are inimical to 
the growth of trees. Even the growth of the grasses, which share dominance with 
Cyperaceae, is sparse and wiry. 


The best-known occurrences of this habitat are at the edges of dambos, the 
seasonally waterlogged grassy depressions which are such a characteristic feature 
of the unrejuvenated plateau surface representing the African cycle of erosion 
(King, 1951) which occupies a large part of the Zambezian Region. 


By far the most extensive occurrences, however, are on the Kalahari Sands 
which occupy the Upper Zambezi basin and its periphery, and extend northwards 
as a narrow belt far into the Guineo-Congolian Region (fig. 3.). The relief of this 
region is so gentle that waterlogged soils occur very extensively in the Zambezi 
basin on the virtually flat interfluves between the lower reaches of the tributary 
rivers of the Zambezi, and, locally, on watersheds of higher elevation which in 
general are better drained. 


This type of anaerobic grassland with suffrutices is the most widespread 
vegetation type in the upper Zambezi basin (White, in press). Apart from the 
dambos mentioned above, it does not occur anywhere else in Africa, except very 
locally. There are small areas associated with impeded drainage in places near the 
coast in the Tongaland-Pondoland Region, which is contiguous with the Zambezian 
Region, and a few suffrutices occur there. 


In the Sudanian Region anaerobic grasslands on sandy oligotrophic soils com- 
parable to those of Zambezia are fragmentary in the extreme, because the land 
surface has reached a different stage in the cycle of erosion. Apart from a few 
small patches scattered along the coast they are confined to small areas, each only 
a few acres in extent, on the flat tops of mesa-like hills where the drainage is 
impeded by the occurrence of hardpan near the surface (J. B. Hall, in litt.). Under 
these circumstances it is difficult to see how a suffruticose flora could have evolved. 


Geoxylic suffrutices are normally absent from secondary grassland following 
the destruction of forest or woodland. They are only plentiful on soils which are 
sO impoverished that they can only support sparse secondary grassland which in 
composition and luxuriance is similar to edaphic suffruticose grassland. This occurs 
chiefly in montane areas and on Kalahari Sand. 


Chapman & White (1970) present evidence which indicates that during the 
last 1000 years extensive areas of montane forest in Malawi have been destroyed 
by fire and replaced by grassland which owing to soil erosion has become pro- 
gressively shorter and less luxuriant. The ultimate stage is a sparse grassland in 
which suffrutices such as species of Protea and Parinari capensis are often con- 
spicuous. According to Fanshawe (1969: 45) sparse grassland with abundant 
suffrutices, which has spread from the waterlogged interfluves and depressions, may 
represent the last stage of degradation of Kalahari forest and woodland following 
clearing and persistent burning. 


64 Gardens’ Bulletin, Singapore — XX1X (1976) 


Kalahari Sand formerly covered a much larger area than it does today as is 
shown by the many residual patches which still survive. 


The great majority of geoxylic suffrutices occurring in the Zambezian Region 
are either confined to the main occurrence of Kalahari Sand centred on Barotse- 
land, e.g. Trichilia quadrivalvis C. De. (fig. 3), or have their centre of distribution 
there, or occur within the range of the former distribution of Kalahari Sands. 

The most abundant species on Kalahari Sand is Parinari capensis, which is also 
the most widespread Zambezian geoxylic suffrutex (fig. 3). It occurs beyond the 
former limits of Kalahari Sand on other types of sandy soil, not only the sandy 


@ 100 200 300 400 500 800 MiLES 
—————— ee 


eS Map of Africa showing distribution of (a) Kalahari Sand (broken line); (b) 
[richilia quadrivalvis C. DC. (continuous line); (c) Parinari capensis Harv. (solid circles). 


: 


Underground Forests of Africa 65 


edges of dambos but also on shallow sandy soils surrounding granite inselbergs in 
the Transvaal and on maritime sands of the Tongaland coastal plain. Most Zambe- 
zian geoxylic suffrutices have distributions intermediate between those of Trichilia 
quadrivalvis and Parinari capensis. 


Evolution 
The significance of fire 


In the absence of fire, some, perhaps most, suffrutices are capable of a limited 
amount of upward growth, but eventually the shoots become moribund and die 
back. Fire destroys this slowly dying, not very floriferous, material, and stimulates 
the production of numerous precociously-flowering shoots. This response to fire is 
clearly adaptive. Flowering takes place some weeks or months before the associated 
grasses, which eventually conceal the suffrutices, begin their growth. Their flowers 
are visible and accessible to pollinating insects and much of the season’s growth is 
completed before competition for light becomes a serious factor. 


It is difficult, however, to see how the suffruticose habit arose in response to 
fire. Chorological and ecological evidence are both against it. 


We have seen that in Africa geoxylic suffrutices have a very uneven distribu- 
tion. The great majority are concentrated in part of the Zambezian Region. The 
Sudanian Region, with various qualifications mentioned elsewhere, is comparable 
in size, climate and flora to the Zambezian. The incidence of fire is the same in 
both, or, if anything, greater in the Sudanian, and yet the latter is almost bereft 
of suffrutices. 


Because of the climatic vicissitudes of the Pleistocene, the Sudanian Region has 
suffered more extinction than the Zambezian, but the disparity between the two 
suffruticose floras, compared with that of some other growth forms, is so great, 
that differential extinction from a former common suffruticose flora provides an 
unlikely explanation. 


Within the Zambezian Region geoxylic suffrutices show a very uneven 
distribution in relation to the intensity of burning. Their most characteristic habitat 
is edaphic grassland, This is a fire-sensitive community and is frequently burnt. But 
it does not burn fiercely, in contrast to most types of secondary grassland occurring 
in the same general area. Suffrutices are conspicuously absent from the latter. It 
has been demonstrated experimentally (Trapnell, 1959, White, unpublished) that 
when Zambezian woodland is subjected to annual fires at the end of the dry season, 
when the burn is more intense, the trees are progressively eliminated, and the grass 
becomes more luxuriant. Suffrutices are not normally found under these conditions. 
Whether fire or competition with the coarse grasses is the primary cause is 
uncertain. The trees may be eliminated as trees, but they are not always killed 
outright. The underground parts survive, and, each year, after the fire, produce an 
annual crop of non-flowering coppice shoots. Even after 40 years of yearly late 
burning, the rootstocks survive and, were the fires to cease, could give rise to trees 
again. Burning as prolonged and intense as this far exceeds the destructive effects 
of natural fires, or fires started in connection with land clearance and farming. 
Lawton (1972) has shown that under the latter conditions many tree species, even 
some which are relatively fire-sensitive, can become established from seed in 
secondary grassland which is subjected to fierce, though not necessarily annual, 
fires. The inescapable fact is that the woodland trees of the Zambezian Region are 
well-adapted to withstand fire — even to withstand a fire-regime far fiercer than 
anything they have experienced in their whole evolutionary history. They have no 
need to evade a menace which does not exist. In some cases the tree which is 
adapted to fierce fires and the related suffrutex which evades them are so similar 
in everything other than pattern of growth and habit that identification is difficult 


66 Gardens’ Bulletin, Singapore — XX1X (1976) 


when the habit is unknown. Examples of such pairs of sibling species are Parinari 
curatellifolia Planch, ex Benth. (tree) and P. capensis, and Diospyros batocana 
Hiern (tree) and D. chamaethamnus Dinter ex Mildbr. It is perhaps significant 
that Parinari curatellifolia is as common in the Sudanian Region as it is in the 
Zambezian, but has not given rise to a suffrutex there. 


The significance of frost 


Burtt Davy’s early account (1922) was concerned with the Highveld in the 
Transvaal. Here the prevalent vegetation is grassland “bare of trees except in the 
shelter of rocky kopjes and even there only a few scattered individuals are met 
with’. A few suffrutices, which also occur on Kalahari Sand, e.g. Dichapetalum 
cymosum, Elephantorrhiza elephantina and Parinari capensis extend into the High- 
veld grassland. A few other suffrutices, e.g. Elephantorrhiza obliqua, Erythrina 
zeyheri and Eugenia pusilla, are more or less confined to it. The winters on the 
Highveld are cold with considerable extremes. Frosts are a regular feature. Killing 
frosts fall as early as March and as late as October. Burtt Davy suggests that in 
the Transvaal the suffruticose habit has evolved in response to frost. This could 
very well be so for the endemic species, but probably less than 10% of the 
suffrutex flora of South Central Africa occur mainly in frosty regions and many 
species occur in or are confined to frost free regions. Other chorological and 
ecological evidence points in another direction. 


Edaphic control 


We have seen that in Africa the great majority of geoxylic suffrutices occur 
on the mantle of Kalahari Sand centred on Barotseland, or within the region of its 
former extent. They are mostly found on sandy soils on very gently sloping or 
almost flat surfaces. The sands, some of which have been redistributed by water, 
are extremely poor in nutrients. Because of the low relief and seasonal climate, 
the sandy soils are seasonally waterlogged and seasonally dry. The fluctuating 
water-table causes the formation of impervious horizons near the surface, This 
accentuates the seasonal differences in soil-water content and restricts the rooting 
environment and hence the nutrient supply of woody plants. In general, seasonally 
waterlogged soils in the same general region favour the growth of grasses vis a vis 
woody plants, but the Kalahari Sands are sometimes so deficient in nutrients that, 
even in the absence of competition from woody plants, the grass growth is sparse. 


The trees of the Zambezian Region cannot withstand seasonal waterlogging 
followed by seasonal drying out of the soil. Under such conditions on the Kalahari 
Sand, and at the sandy edges of dambos on the Central African plateau, trees are 
replaced by suffrutices. Where flooding is prolonged, woody plants are completely 
excluded. 


Except when the suffrutices are flowering, the communities they occur in have 
the appearance of grassland and are usually described as such. The phytomass of 
the suffrutices however greatly exceeds that of the grasses. 


The correlation between the edaphic conditions just described and the distribu- 
tion of geoxylic suffrutices is so great, and the correlation between the incidence 
of fire and the incidence of frost and the occurrence of suffrutices so weak, that 
we must postulate a causal connection for the former. We must also look for 
confirmatory evidence. 


Although edaphic grassland with suffrutices is the most extensive vegetation 
type in the upper Zambezi basin, dry forest (now largely destroyed) occurs on the 
deeper well-drained sands, and is separated from the edaphic grassland by an 
ecotone of woodland and wooded grassland, 


I 


; 


Underground Forests of Africa 67 


Within the upper Zambezi basin there is a complex mosaic of different edaphic 
conditions largely dependent on effective depth of soil and its water-relations. It 
is under circumstances such as these, especially where soil fertility is at a critical 
low level, that one would expect to find intermediate stages in the evolution of the 
suffruticose habit. The best example is provided by Baikiaea plurijuga Harms. 


Baikiaea is a small genus of trees which is confined to the Guineo-Congolian 
Region, except for B. plurijuga which dominates dry semi-deciduous forest on deep 
well-drained Kalahari Sand in the lower half of the upper Zambezi basin. The 
northernmost occurrences of B. plurijuga are separated from the Guineo-Congolian 
Region by an interval of 600 km. B. plurijuga is normally a tree 20 m. or more in 
height. There are no suffruticose species of Baikiaea, but B. plurijuga has recently 
(Fanshawe & Savory, 1964) been found to occur on sites which appear to be 
intermediate between typical forest sites and typical suffruticose grassland. Here 
Baikiaea forms dwarf forests less than 2 m. tall. “If the root is excavated a 
candelabra effect is exposed”. Just below the soil surface the original tap root gives 
off a number of comparatively short twisted branches from the ends of which 
tufted shoots arise. The latter apparently persist for no more than 4 years. This 
life-form of Baikiaea is very similar to that of a rhizomatous geoxylic suffrutex. 
Fanshawe and Savory suggest that the curious growth-form of Baikiaea might be 
due to a peculiarity of nutrient status but is more likely to be due to impeded 
drainage. A more detailed study of the edaphic conditions would be most 
instructive. 


A change in growth-form as drastic as that between a forest tree and a 
geoxylic suffrutex could not be caused by the tree invading a new and very 
different habitat under a stable environment, followed by its descendants gradually 
adapting to the different conditions by mutation and selection. The original invader 
would be eliminated by selection from the start. Such a change is much more likely 
to happen if the environment of a population undergoes a gradual change to which 
the population gradually adapts. In a region of such low relief and imperfect 
drainage as Barotseland, relatively little change, either climatic or physiographic, 
would be necessary to bring this about. Indeed, in another publication, Fanshawe 
(1969b) discusses evidence which suggests that in one part of Barotseland the 
water-table is at present rising and causing the deaths of trees over a large area. 


It is currently fashionable to interpret most patterns of plant distribution in 
Africa and some patterns of taxonomic relationship, especially where closely 
related species are involved, in terms of climatic events of the Pleistocene, very 
often in terms of the most recent phases, involving a period of no more than 
20,000 years. Much, doubtless, can be interpreted in this way, but much cannot. 
It is likely that edaphic conditions favourable for the evolution of suffrutices were 
greatly extended in Barotseland during the pluvial periods of the Pleistocene, but 
this does not mean that the suffrutices originated then. Quite small physiographic 
events such as minor warping of the earth’s crust or the capture of major tributary 
rivers could produce, over quite extensive areas, the kind of edaphic change 
required for transformation in growth form. This could have happened repeatedly 
over a very long period of geological time. The genus Parinari, which has figured 
sO prominently in this discussion, is well represented in tropical America, Africa 
and Asia, and occurs in Madagascar. In its leaves, flowers and fruits it is remarkably 
uniform, and has diversified little since the breakup of Gondwanaland. Is it 
necessary to postulate that its speciation occurred in the Pleistocene? Is it not more 
likely that the tumultuous events of that period have merely sharpened the edges 
of taxa which began their differentiation a very long time before? 


68 Gardens’ Bulletin, Singapore — XXIX (1976) 


APPENDIX 


Systematic List of Obligate and Facultative Geoxylic Suffrutices occurring in Africa. 


S — occurring in Sudanian Region. T-P — occurring in Tongaland-Pondoland Region. 


Z — occurring in Zambezian Region. 


ANACARDIACEAE 


Z. Heeria nitida Engl. & v. Brehm. and 
c. 8 other species 


Z. Lannea edulis (Sond.) Engl. 
Z. L. gossweileri Exell & Mendonca 
Z. L. katangensis Van der Veken 
Z. L. virgata R & A. Fernandes 
Z. Rhus kirkii Oliv. and c. 4 other 
species 
ANNONACEAE 


Z. Annona stenophylla Engl. & Diels 


APOCYNACEAE 
Z. Chamaeclitandra henriquesiana (K. 
Schum. ex Warb.) Pichon 


Z. Landolphia gossweileri (Stapf) Pichon 
— facultative; liane 


Z. Rauvolfia nana E. A. Bruce 
Z. Strophanthus angusii F. White 


ARALIACEAE 
Z. Cussonia corbisieri De Wild. 
CELASTRACEAE 
Z. Salacia bussei Lozs. — facultative; 
shrub 


Z. S. luebbertii Loes. 
T-P. S. kraussii— (Harv.) Harv. — facul- 
tative; shrub 
CHRYSOBALANACEAE 
Z. Magnistipula sapinii De Wild. 
Z. Parinari capensis Harv. 


COCHLOSPERMACEAE 
S. Cochlospermum tinctorium A. Rich. 


COMBRETACEAE 
Z. Combretum argyrotrichum Welw. ex 
Laws. 
brassiciforme Exell 
. harmsianum Diels 
. lineare Keay 
. platypetalum Welw. ex Laws. 
. relictum Hutch & Dalz. 
. sericeum G. Don f. 
viscosum Exell 


DICHAPETALACEAE 


Z. Dichapetalum bullockii Hauman 
Z. D. cymosum (Hook.) Engl. 
Z. D. rhodesicum Sprague & Hutch. 


NwANYY 
QAAANAANAA 


DILLENIACEAE 
Z. Tetracera masuiana De Wild. & Th. 
Dur. 


EBENACEAE 


Z. Diospyros chamaethamnus Dinter ex 
Mildbr. 


, T-P. D. galpinii Hiern 
, I-P. D. lycioides Desf. — faculta- 
tive; shrub, small tree 


D. virgata (Giirke) Brenan 
Euclea crispa (Thunb.) Giirke — 
facultative; shrub, small tree 
FLACOURTIACEAE 
Z. Caloncoba suffruticosa (Milne-Redh.) 
Exell & Sleumer 
GUTTIFERAE 
Z. Garcinia buchneri Engl. 
Z. Psorospermum mechowii Engl. 


IXONANTHACEAE 
Z. Ochthocosmus candidus (Engl. & 
Gilg) Hall. f. 
LECYTHIDACEAE 
Z. Napoleona gossweileri Baker f. 


LEGUMINOSAE: CAESALPINIOIDEAE 
Z. Brachystegia russelliae Johnston 


Z. Cryptosepalum exfoliatum De Wild, 
— facultative, small tree 


Z. OC. maraviense Oliv. 


LEGUMINOSAE: MIMOSOIDEAE 


Z, T-P Elephantorrhiza elephantina 
(Burch.) Skeels 


Bs E. obliqua Burtt Davy 

T-P E. woodii Phillips 

Ph Entada dolichorrhachis Brenan 
7 E. nana Harms 


LEGUMINOSAE: PAPILIONOIDEAE 


Z. Erythrina baumii Harms 
Z. EE. zeyheri Harv. 


NN NN 


LINACEAE 
Z. Hugonia gossweileri Bak. f. & Exell 
ex De Wild. 
LOGANIACEAE 
Z. Strychnos gossweileri Exell — facul- 
tative; liane 
MALPIGHIACEAE 


Z. Sphedamnocarpus angolensis (A. 
Juss.) Planch. ex Oliv. 
MELIACEAE 


Z. Ekebergia pumila 1. M. Johnston 
Z. Trichilia quadrivalvis C. DC. 


Underground Forests of Africa 


MORACEAE 
Z. Ficus pygmaea Welw. ex Hiern 
Z. F. verruculosa Warb. — facultative; 
small tree 
MYRTACEAE 


Z. Eugenia angolensis Engl. 


T-P E. capensis (Eckl. & Zeyh.) Sond. 
— facultative; tree 


Z. E. pusilla N. E. Br. 
Z. Syzygium guineense (Willd.) DC. 
subsp. hAuillense (Hiern) F. White 


OCHNACEAE 


Z. Brackenridgea arenaria (De Wild. & 
Dur.) N. Robson — facultative; 
shrub. 


Ochna confusa Burtt Davy & Green- 
way 


O. katangensis De Wild. 
O. leptoclada Oliv. 


O. macrocalyx Oliv. — facultative; 
shrub 


O. manikensis De Wild. 


Ochna mossambicensis Klotzsch — 
facultative; shrub 


O. pygmaea Hiern 
O. richardsiae N. Robson 


PASSIFLORACEAE 

Z. Paropsia brazzeana Baill. — faculta- 

tive; shrub 

PROTEACEAE 

Z. Protea angolensis Welw. 

Z. P. heckmanniana Engl. 

Z. P. paludosa Welw. 

Z. P. trichophylla Engl. & Gilg 
RHAMNACEAE 

Z. Ziziphus zeyherana Sond. 


NN NN NNN N 


69 
RHIZOPHORACEAE 
Z. Anisophyllea quangensis Engl. ex 
Henriques 
RUBIACEAE 


Z. Ancylanthus rubiginosus Desf. 
Gardenia subacaulis Stapf & Hutch. 


Leptactina benguelensis (Welw. ex 
Benth. & Hook. f.) R. Good 


Morinda angolensis (R. Good) F. 
White 

Pachystigma pygmaeum_ (Schlecht.) 
Robyns 

Pavetta pygmaea Brem. 

Psychotria spp. 


*Pygmaeothamnus concrescens 
Bullock 


P. zeyheri (Sond.) Robyns 
Tapiphyllum spp. 

Tricalysia cacondensis Hiern 
T. suffruticosa Hutch. 


SANNA NNN & NP 


SAPINDACEAE 
Z. Deinbollia fanshawei Exell 


TILIACEAE 


Z. Grewia decemovulata Merxm. — 
facultative; shrub 

Z. G. falcistipula K. Schum. — faculta- 
tive; shrub 


Z. G. herbacea Welw. ex Hiern 


VERBENACEAE 
Z. Clerodendrum buchneri Giirke 
Z. C. lanceolatum Giirke 
Z. C. milne-redheadii Moldenke 
Z. C. pusillum Giirke 
Z. C. triplinerve Rolfe 


* This genus only has suffruticose members. It is however very closely related to the 


arborescent Canthium. 


70 Gardens’ Bulletin, Singapore — X XIX (1976) 


References 


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CHAPMAN, J. D. & F. WHITE. 1970. The evergreen forests of Malawi. Comm. 
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DU RIETZ, G. E. 1931. Life-forms of terrestrial flowering plants, I. Act. a 
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DUVIGNEAUD, P. 1954. Une Erythrine 4 xylopode des steppes du Kwango. 
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EXELL, A. W. & C. A. STACE. 1972. Patterns of distribution in the Combretaceae. 
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1969b. The vegetation of Kalabo District. For. Res. Pamphl. 22. 
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& B. M. SAVORY. 1964. Baikiaea plurijuga dwarf-shell forests. 
Kirkia 4: 185-190. 


HALLE, F. & R. A. A. OLDEMAN. 1970. Essai sur l’architecture et la dynamique 
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KING, L. C. 1951. South African scenery, ed. 2. Oliver & Boyd, Edinburgh. 


LAWTON, R. M. 1972. An ecological study of miombo and chipya woodland with 
particular reference to Zambia, Thesis, Oxford University. 


MABBERLEY, D. J. 1974a. Branching in pachycaul Senecios: the Durian Theory 
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1974b. Pachycauly, vessel-elements, islands and the evolution of 
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MANGENOT, G. 1969. Réflexions sur les types biologiques des plantes vascu- 
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PRANCE, G. T. 1972. Fl. Neotropica Monogr. 9, Chrysobalanaceae. Hafner, New 
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& M. FREITAS da SILVA. 1973. Fl. Neotropica Monogr. 12, 
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RAWITSCHER, F. K., M. G. FERRI & M. RACHID. 1943. Profundidade dos 
solos e vegetacdo em campos cerrados do Brasil Meridional. Anais. Acad. 
bras. Cienc. 15: (4). 


& M. RACHID. 1946. Troncos subterrancos de plantas Brasileiras. 
Anais. Acad. bras. Cienc. 18: 261-280. 


SCHIMPER, A. F. W. 1898. Pflanzen-Geographie auf physiologischer Grundlage. 
Fischer, Jena. 


Underground Forests of Africa 71 

TRAPNELL, C. G. 1959. Ecological results of woodland burning experiments in 
Northern Rhodesia. J. Ecol. 47: 129-168. 

WARMING, E. 1892. Lagoa Santa. 


WHITE, F. 1962. Geographic variation and speciation in Africa with particular 
reference to Diospyros. Syst. Assn Publ. 4: 71-103. 


1965. The savanna woodlands of the Zambezian and Sudanian 
Domains: an ecological and phytogeographical comparison. Webbia 19: 
651-681. 


(ed.) (in press). Vegetation map of Africa. UNESCO, Paris. 


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Notes on Rain-Forest Herbs 


by 
B. L. BURTT 


Royal Botanic Garden, Edinburgh 


Concise summaries of views on the herbaceous plants of rain-forest have been 
given by Richards (1952, pp. 96-102) and by Walter (1971, pp. 118-122). The 
present notes are an attempt to expand the subject a little further, by recording 
some observations on the growth patterns of dicotyledonous herbs and emphasising 
the contrasts both with monocotyledons and with temperate forest dicotyledons. 
At present the relation between structural features of the leaves and physiological 
function is, in general, rather uncertain, and this is not the field for a taxonomist 
to enter. Nevertheless I have ventured a few remarks, if only as a reminder of the 
questions a field-botanist wants to ask. These notes are inevitably limited by my 
personal experience, which wholly excludes the New World and is derived largely 
from collecting trips in Sarawak. 


The importance of the massive tropical palms (Palmae) and screw-pines 
(Pandanaceae) in attaining a balanced appreciation of monocotyledons as a group 
is now widely recognized. But even at the level of rain-forest herbs a comparison 
between monocotyledons and dicotyledons illuminates some fundamental differences 
more brightly than a similar study in temperate forests. When these are brought 
into the picture, it is immediately apparent that, under the impact of a strongly 
seasonal climate, the contrast between monocotyledon and dicotyledon has been 
lessened. 


First let us look at growth-habits, particularly at the underground parts. In 
temperate forests rhizomes or stolons with scale-leaves are frequent, both amongst 
dicotyledons and monocotyledons: for instance, Mercurialis (Euphorbiaceae — see 
Mukherji, 1936) or Paris (Liliaceae — see Kirchner, Loew & Schroter, 1934) in 
Europe; Podophyllum (Berberidaceae — see Holm, 1899) or Medeola (Liliaceae 
— see Bell, 1974) in North America. Examples could easily be multiplied. 


Of the herbs of tropical rain-forest Richards (1952, p. 98) says “ ... plants 
with underground rhizomes are frequent, but the rhizomes are adapted for multi- 
plication and migration rather than perennation”. He is echoed, despite a slightly 
different concept of perennation, by Walter (1971, p. 118): “‘the herbs are often 
equipped with underground perennating organs such as rhizomes and tubers. But 
these serve less as storage organs for reserve food than as a means of vegetative 
reproduction”. These statements need some qualification. They might seem to 
imply, no doubt unintentionally, that the rhizomes of temperate forest herbs do 
not serve for spread or vegetative reproduction; of course, they clearly do so. 
Secondly, in my experience, rhizomes may be common on tropical monocotyledons 
but they are certainly very rare amongst the dicotyledons. In considering rain-forest 
herbs the two groups must be distinguished. 


It may be as well to restrict the words “storage” and ‘‘perennation” to use 
when a seasonal dormancy is accompanied by complete die-back of aerial shoots. 
Then the situation found in most non-seasonal rain-forest herbs with underground 
rhizomes may be described as the accumulation of food-reserves. The importance 
of this must not be underestimated in the monocotyledons. The rhizomes of many 


73 


74 Gardens’ Bulletin, Singapore — X XIX (1976) 


Zingiberaceae eventually throw up massive new leaf-fronds anything from 1.5 to 
9 metres in height. This can scarcely be achieved without the backing of some 
accumulated reserves, even though there is continuity through the rhizome or stolon 
to older actively photosynthetic fronds. Very often the tip of the rhizome becomes 
decidedly swollen when it turns up to form the new leaf-frond. 


Some Zingiberaceae grow in tight clumps, and these, of course, have short 
slow-growing rhizomes; others form dense or diffuse patches, and in these the 
rhizome is extended as a far-ranging stolon. Apart from question of size, the 
patterns are those of rhizomatous herbs in temperate forests. 


Dicotyledonous herbs also form patches in the rain-forest, but this is achieved 
without the aid of scale-clad underground rhizomes or stolons. A characteristic 
pattern of growth can be observed in Cyrtandra radiciflora C.B.Cl. (Gesneriaceae). 
This species forms stands with erect leafy shoots keeping a more or less even height 
of about 0.75 metre. These shoots are evergreen and their duration is unknown. 
Flowering is axillary and basal, at or near ground level. The terminal bud remains 
vegetative and produces a succession of leaves. What prevents the shoots from 
growing higher and higher? 


It seems that the average height is maintained because, as upwards growth 
proceeds, the lower part of the stem becomes more and more decumbent. If a 
handful of shoots are pulled up it will be found that they are linked by pieces of 
prostrate, sometimes buried, stem. Buds on the prostrate stems give rise to new 
shoots that help to thicken the patch, and the process of becoming prostrate helps 
to expand it. At all times the main growing points of the shoots are aerial and are 
directed upwards. There is no horizontal (diageotropic) growing point like that 
of a rhizome or stolon. 


The pattern just described for Cyrtandra radiciflora is found in a number of 
species of this genus (which is very large and very varied in growth-patterns), and 
in other genera where some species have axillary inflorescences: Argostemma 
(Rubiaceae), Elatostema (Urticaceae), Linariantha (Acanthaceae), Gomphos- 
temma (Labiatae) come to mind. Other rain-forest herbs (e.g. some Acanthaceae) 
have terminal inflorescences; these plants retain their herbaceous stature by dying 
down to near the base after fruiting and form new shoots from basal buds: scars 
of old shoots are often visible, though I have never noticed a dead shoot in situ. 
Observations on the death-patterns of tropical herbs are badly needed: there are 
indications that the fruiting shoot may die slowly, so that its leaves are still 
photosynthetic long after the seeds are shed. This could be a necessary feature, in 
the absence of underground storage organs, to support the growth of a new shoot: 
but that is speculation until careful studies can be made. This pattern of growth 
is shown in some forest species of Pseuderanthemum (Acanthaceae); other members 
of the genus do not die back but produce shoot-buds from the axils of leaves just 
below the dead infructescence — and become shrubs, Another genus of Acanthaceae 
which has terminal inflorescences and dies down is Cosmianthemum; it is unusual 
in having somewhat fleshy roots; otherwise the roots of these forest herbs are thin 
and wiry. 


By no means all the dicotyledons with axillary flowers become decumbent at 
the base. A very frequent habit is a stiff erect unbranched stem with the leaves 
tending to be in the upper part, sometimes in a distinct cluster near the top — 
rather the habit of a miniature palm tree. Once again we have no knowledge of the 
duration of such plants. This habit is found in a number of genera, for instance 
Didymocarpus, Didissandra and Cyrtandra (Gesneriaceae), Sonerila (Melasto- 
maceae) and Neckia (Ochnaceae). 


A simple modification is found when species grow horizontally from vertical 
cliff faces; then the terminal tuft of leaves is eccentric, the leaves on the lower side 


being longer; in Cyrtandra mirabilis C.B.Cl. the longest leaves may be as much as : 


Rain-forests herbs 75 


70 cm, and as they are thin and delicate this would be an impossible size on an erect 
stem. In this habitat, too, is found an elaboration of the simple pattern; the stem 
is branched, each branch having its characteristic tuft of leaves: in a form of 
Didymocar pus gracilipes C.B.Cl. there may be as many as 20 leaf-tufts. Again it 
is difficult to envisage this pattern being successful as an erect stem. Cliff-plants 
with these fans of pendulous leaves are found in both Asiatic and American 
Gesneriaceae (cf. Resia H. E. Moore, 1962), and also in such genera as Steenisia 
(Rubiaceae). 


Another variant is the plant with an erect fan of leaves sometimes found on 
steep slopes and banks in the forest. Here the stem is short, or the lower part 
becomes prostrate keeping the leaf tuft near ground level. Such a fan of leaves, 
each about 30 cm long, is beautifully shown in Cyrtandra penduliflora Kraenzl. and 
is associated there with marked anisophylly—one leaf of each pair is reduced to a 
small stipule-like structure — and the development of prop roots, perhaps 20-30 cm 
long and 2 mm diam. quite rigid and branching only when they have reached the 
soil. These are of obvious value in supporting the plant in steep habitats. 


It might seem that the simple erect stem and the decumbent, branched, patch- 
forming type stand widely apart. However, Didymocarpus malayanus Hook. f. is 
a plant of the Malay Peninsula which occurs in two forms: one has an erect 
unbranched stem, but the leaves show rather less apical aggregation than charac- 
teristic of that pattern, while the other is a prostrate mat-forming type, the shoots 
never being more than about 6 inches above the surface of the ground. Although 
the inflorescences of the erect plant carry many more flowers, there appears to be 
no essential difference between the two: if eventually separable as distinct species, 
they are at least very closely allied. 


One noteworthy type of growth that I have not personally encountered in 
Sarawak (and I think it is not recorded there) is the much branched monocarpic 
herb represented by several species of Strobilanthes (Acanthaceae). These plants 
are well known for their gregarious habit and their periodic simultaneous flowering. 
Records for Sumatra and Java are summarized by van Steenis (1942); they include 
S. kunthianus Benth. from open grassy places and S. cernuus Bl. and others which 
are “‘hygrophytes of rather dark mountain forests’. The habit is best known in 
species of Strobilanthes found in the seasonal forests of India, and also occurs in 
other genera of Acanthaceae (Isoglossa, Mimulopsis) in the evergreen but distinctly 
seasonal forests of eastern and south-eastern Africa. 


In these seasonal forests underground storage organs become much more 
frequent in dicotyledons: climbers with annual stems and tubers become prominent 
(Gerrardanthus, Cissus fragilis Harv., Tacazzea in Natal) and genera which lack 
storage organs in rain-forest, or in the always-damp habitats in these seasonal 
forests, develop them: for instance Begonia. In south-east Africa Impatiens 
duthieae L. Bolus is found in always-damp situations in the forest and has no 
storage organs, J. flanaganae Hemsl., more exposed to seasonal change at the forest 
margin, has tubers; in northern Malaya Impatiens mirabilis Hook. f., a plant of 
the somewhat seasonal forests on the limestone, has a thickened storage trunk 
resembling an Adenium. 


Two genera of monocotyledons that range from the seasonal monsoon forests 
of south-east Asia down into the rain-forest are particularly interesting. These are 
Arisaema (Araceae) and Hedychium (Zingiberaceae). By far the greater number 
of the species of Arisaema live under markedly seasonal conditions: they have an 
underground corm which produces leaves and inflorescence annually and has a 
distinct period of rest. This pattern is found also in Arisaema fimbriatum Mast. of 
the Langkawi Islands, N. Malaya, where the forest is largely evergreen, but with 
a proportion of deciduous species and a distinctly dry and cool winter. Species 
are found further south on the mainland (A. anomalum Hemsl.) and in Borneo 


76 Gardens’ Bulletin, Singapore — X XIX (1976) 


and Java (A. umbrinum Ridl., A. filiforme Bl. etc.), which have a thick fleshy 
rhizome, rather than a corm, and these plants have leaves present all the year 
round. Hedychium is rhizomatous throughout its range, but in the northern seasonal 
area all the leaf fronds die down in winter and the plant is dormant; in the 
Bornean H. cylindricum Ridl. there are leaf fronds present throughout the year. 


Another aroid, Amorphophallus, seems to be somewhat anomalous in its 
behaviour. It has a large corm and Walter (1971, p. 118) reports that in Africa, 
where it grows in seasonal areas, it flowers before it leaves. In Sarawak, where 
it is by no means uncommon, a corm will produce a flower in one year, a leaf in 
another: adjacent corms are in growth simultaneously so that flowers and leaves 
may be found together. However there is probably no strict alternation of flowering 
and leafing years: it seems likely that flowering only takes place at intervals of 
several years; one can see 50 plants in leaf for every one with an inflorescence, In 
any case Amorphophallus is, I think, unique among the rain-forest herbs in having 
a well-marked annual dormancy. 


To return to the comparison of monocotyledons and dicotyledons, we find that 
rhizomes and stolons with scale leaves are virtually restricted, in the rain-forest, 
to the monocotyledons. The dicotyledons lack subterranean, or superficial, shoots 
with scale leaves and diageotropic growing points. As these features are well known 
amongst the dicotyledons of temperate forests, it is reasonable to suppose that they 
have been developed there in response to a markedly seasonal climate. In the 
monocotyledons they seem to be part of the normal developmental pattern of the 
plants: their well developed scales represent only the sheaths of the mature leaf 
and remind us that in the monocotyledons the sheath is a much more important 
part of the leaf than it is in the dicotyledons, where it is well-developed only 
sporadically in quite diverse families (Umbelliferae, Polygonaceae etc.). The 
important role of the rhizome in monocotyledons is perhaps another aspect of 
growth linked to their fundamentally hypogeal pattern of germination (cf. Burtt, 
1972). 


Many of the dicotyledonous herbs of the forest floor have small seeds; such 
are all the Gesneriaceae, Begonia, some Rubiaceae and a few Acanthaceae (e.g. 
Staurogyne). Such seeds are probably dispersed by rainwash or by carriage on the 
feet of animals, and these two methods probably provide the best chance of 
dispersal under rain-forest conditions. Small seeds may also be favoured by the 
fact that they do not offer a desirable food-store to seed-predators. Salisbury’s 
comparative study of seed size in relation to open and woodland habitats in 
temperate Europe showed that amongst closely related species those of shady 
habitats had larger seeds. Such a comparison is scarcely possible in Sarawak where 
the primary vegetation of virtually the whole country is forest. 


The advantages of small seeds in rain-forest, suggested above, may be enough 
to outweigh the limitations imposed by the seedling having to start life with a very 
small capital of food reserves. These limitations would, however, exert a selection 
pressure in favour of any seedling strategy that evaded or ameliorated them, I have 
suggested elsewhere (Burtt, 1970) that this is just what is achieved by the continued 
post-germination growth of one cotyledon in Gesneriaceae. The enlarged photo- 
synthetic surface enables the seedling to build up energy for the organization of the 
plumular bud, which is delayed by comparison with its rapid appearance in most 
plants. The fungal association formed by the roots of the microspermous orchids 
is, Of course, another way in which this difficulty is overcome, and the same 
argument may be applied to a widespread dicotyledonous saprophyte of the Malesian 
rain-forest, Cotylanthera (Gentianceae). In another microspermous family of 
monocotyledons, Burmanniaceae, both (fully?) autotrophic (Burmannia longi- 
folia Becc.) and heterotrophic species (B. sphagnoides Becc., etc.) are found in the 
forest, but here the heterotrophic association is with blue-green algae, not with 
fungi. 


Rain-forests herbs 77 


Begonia is a microspermous genus of herbs in tropical forests all over the 
world. It does not seem to have any means of offsetting this disadvantage of small 
seeds: yet although Begonia plants are common, and seed-setting apparently 
prolific, seedlings are in my experience (which I admit is inadequate) curiously 
rare — especially as collected seed germinates freely in the greenhouse. This, of 
course, is not a situation affecting Begonia alone. Seedlings of herbaceous plants 
are so uncommon in the rain-forest that very little can be said about them. However 
the situation is similar, but perhaps a little less pronounced, in temperate forests, 
so this is not a rain-forest peculiarity. Nonetheless their rarity in the very open 
vegetation of the forest floor is noteworthy and needs investigation. 


To this seedling rarity there are a few exceptions. Seedlings of two genera of 
Gesneriaceae are not infrequent, sometimes very prolific, in rocky forests on 
limestone. These genera are Monophyllaea and Epithema, We do not know the 
exact duration of the normal life cycle of these plants but it is certain that in both 
genera it is relatively short. In other words seedlings occur plentifully when they 
are necessary for the maintenance of the species. We are reminded that the 
biennial Digitalis purpurea L. produces seedlings freely in European woodlands, 
while young plants of Primula vulgaris Huds. need to be carefully sought. Similarly 
in subtropical evergreen kloof forests near Durban, Natal, the short-lived mono- 
carpic Streptocarpus molweniensis Hilliard (Gesneriaceae) produces myriads of 
seedlings. Thus reproduction by seed seems to present similar problems for investi- 
gation in forest herbs under a wide range of climatic conditions. 


If there is one lesson to be learnt from the history of botany, it is surely that 
attempts to give physiological explanations of leaf-structure without adequate 
physiological experiment are extremely hazardous. And physiological experiments 
in tropical rain-forest have so far been quite inadequate both in precision and in 
the range of subject used. All I can do here is to abstract some current thought 
from the physiological literature and try to relate it to the features I have seen in 
rain-forest herbs. If it spurs someone to write an authoritative account I shall be 
more than satisfied. 


Even the physical measurements of the environment are very difficult in rain- 
forest (cf. Schulz, 1960); however it seems probable that the following conditions 
often obtain near the forest-floor. There is a low or very low saturation deficit; the 
carbon dioxide concentration is somewhat above normal (though not as high as 
was at one time suggested); average light intensities are low; and the incidence and 
intensity of sun-flecks, leading to sudden rises in leaf-temperatures, are a factor 
of great physiological significance (Evans, Whitmore & Wong, 1962). In this latter 
connexion Evans (1972, p. 34) has emphasized the extreme complexity of leaf 
temperatures, the extent of changes and their effects. 


As to the plants’ behaviour under these conditions, the early hypothesis of 
Stahl (1896) has now been abandoned: it was that a high transpiration rate was 
necessary to permit adequate salt absorption from weak soil solutions, and he 
interpreted various structural peculiarities as aiding this high transpiration rate. 
It is now known, from greenhouse studies, that an increase in the CO, concentration 
not only enhances assimilation, but lowers the transpiration rate (Hughes 1966; 
Meidner & Mansfield 1968, p. 76). Plants on the forest floor actually have very 
low transpiration rates (McLean 1919, Walter 1971): so this feature harmonizes 
with the higher CO, concentrations found there. 


Rain-forest herbs have typical shade-leaf histology in that they are thin and 
the palisade often consists of only a single layer of shallow cells. However a more 
specifically rain-forest feature is the frequent occurrence of a well-developed water- 
storing hypodermis, or in its absence the epidermis itself is large-celled and aqueous 
(for notes on Cyrtandra see Bokhari & Burtt, 1970). It has been shown (McLean, 
1919) that development of conducting tissue in rain-forest herbs is relatively weak. 


78 Gardens’ Bulletin, Singapore — XX1X (1976) 


One is tempted to link water storage to the sudden effects of sun-flecks on the one 
hand and poorly developed xylem on the other: but no experimental work in this 
field is known to me. Nor, as far as I am aware, has the working of stomata on 
raised “turrets” (common in Gesneriaceae, and see the illustration of Ruellia in 
Strasburger, 1965) been studied experimentally. Until we know how they affect 
transpiration when they are open, and how often they are open, speculation can 
only be wild. 


Leaf-surface is of considerable interest amongst rain-forest herbs. Not 
infrequently the upper surface is thrown up into numerous small peaks with 
corresponding hollows below; this is the condition usually described as “‘mammil- 
late’. It occurs, at least, in some species of Cyrtandra and Didymocarpus 
(Gesneriaceae), and Begonia (Begoniaceae), and in Tropical America species of 
Pilea (Urticaceae) show the same feature. The palisade tissue is continuous over 
these peaks and thus its quantity is increased within a given leaf area. Although 
the direct incident light on that area remains the same, it may be that this type 
of surface permits the plant to make better use of the lateral component of the 
lighting. It would be interesting to compare the assimilation of smooth and 
mammillate leaves when direct illumination is excluded. 


Another well-known feature of certain plants growing in deep forest shade is 
their blue-green iridescence. Lee & Lowry (1975) have recently returned to a study 
of this phenomenon and now suggest that the iridescence is produced by a 
structural layer in the wall of the epidermis which increases the reflection of light 
rays in that part of the spectrum that is of least value in photosynthesis, but 
enhances the penetration of the most useful wavelengths. Selaginella is probably 
the commonest plant showing this iridescence, but it is also found in flowering 
plants such as Begonia and is very well-marked in Mapania (Cyperaceae). 


Leaf colour in forest herbs is a subject that has attracted much speculation; 
but I have not found much detailed information in the literature on its occurrence. 
The phenomena generally discussed are red coloration in general and red-green or 
silver-green mottling; adaptive advantages have been sought for these conditions. 
It is therefore worthwhile to put on record that any advantage that they do confer 
on the plant has often been inadequate for them to become constant within the 
species concerned. For instance, closely adjacent or mixed populations of Sonerila 
tenuifolia Bl. (Melastomataceae) may be found with green or purple leaves, either 
colour being with or without whitish blotches; some Begonia species occur in 
colonies showing a mixture of blotched and unblotched leaves; Sonerila borneensis 
Cogn. may have leaves of plants growing within a short distance of one another 
silver-streaked or plain green, and the same applies in Monophyllaea glauca C.B.Cl. 
var., in which silvering, when present, is more conspicuous in the seedling phase. 
Similarly in Cyrtandra splendens C.B.Cl. plain green leaves, leaves mottled in darker 
and lighter green, leaves flushed or wholly coloured red on the underside or leaves 
red on both surfaces seem to occur indiscriminately. It is also well known that 
some ‘forms’ of the species popular for greenhouse cultivation have leaves more 
spectacularly coloured than others (e.g. cultivars of Episcia reptans Mart. — 
Gesneriaceae — and Bertolonia — Melastomataceae). Little emphasis has been 
placed on the implication of intraspecific variation when considering the possible 
adaptive significance of these colour patterns. This is not to deny that they may 
be adaptive, and in some species (e.g. in Dossinia marmorata Bl., or in the 
light and dark green mottling of many species of Paphiopedilum, both Orchidaceae) 


they do seem to be constant, But the examples of inconstancy within a species are 
too frequent to be ignored. 


Rain-forests herbs 79 


One thing is clear in this physiological uncertainty: that the forest-floor 
environment in evergreen tropical forest is far from optimal. Richards (1952, 
p. 98) has emphasized this, and points to the relatively low number of families 
represented in the herbaceous flora. It will have been noted how often the genera 
Begonia, Cyrtandra, Didymocarpus, Argostemma, Sonerila have recurred as 
examples; this is partly due to my limited experience but it does also demonstrate 
that these large genera have shown parallel evolutionary diversification to cover 
several successful growth-forms. There is scope for an interesting study in assessing 
how many groups of genera have representatives in, or are wholly confined to, 
the herbaceous flora of the rain-forests and the extent of their diversification there. 


References 


BELL, A. 1974. Rhizome organization in relation to vegetative spread in Medeola 
virginiana. J. Arnold Arbor. 55: 458-468. 


BOKHARI, M.H. & B. L. BURTT. 1970. Studies in the Gesneriaceae of the Old 
World XXXII: Foliar sclereids in Cyrtandra. Notes R. bot. Gdn Edinb. 
30: 11-21. 


BURTT, B. L. 1970. Studies in the Gesneriaceae of the Old World, XXXI: Some 
aspects of functional evolution. Notes R. bot. Gdn 30: 1-10. 


1972. Plumular protection and some related aspects of seedling 
behaviour. Trans. bot. Soc. Edinb. 41: 393-400. 


EVANS, G. C. 1972. The quantitative analysis of plant growth. Blackwell, Oxford. 


EVANS, G. C., T. C, WHITMORE & Y. K. WONG. 1962. The distribution of 
light reaching the ground vegetation in a tropical rain-forest. J. Ecol. 
48: 193-204. 


HOLM, T. 1899. Podophyllum peltatum: a morphological study. Bot. Gaz. 
27: 419-434. 


HUGHES, A. P. 1966. The importance of light compared with other factors 
affecting plant growth. In Bainbridge, R., Evans, G. C. & Rackham, O. 
Light as an ecological factor, pp. 121-146. Blackwell, Oxford. 


KIRCHNER, O. von, E. LOEW & C. SCHROTER. 1934. Lebensgeschichte der 
Bliitenpflanzen Mitteleuropas 1 (3): 645. 


LEE, D. W. & J. B. LOWRY. 1975. Physical basis and ecological significance of 
iridescence in blue plants. Nature (Lond.) 254: 50-51. 


McLEAN, R. C. 1919. Studies in the ecology of tropical rain-forest. J. Ecol 
7: 5-54, 121-172. 


MEIDNER, H. & T. A. MANSFIELD. 1968. Physiology of stomata. McGraw 
Hill, London. 


MOORE, H. J. 1962. Resia — a new genus of Gesneriaceae. Bot. Mus. Leafl. Harv. 
Univ. 20: 85. 


MUKERII, S. K. 1936. Contribution to the autecology of Mercurialis perennis L. 
J. Ecol. 24: 36-81. 


RICHARDS, P. W. 1952. The Tropical Rain Forest. University Press, Cambridge. 


SCHULZ, J. P. 1960. Ecological studies on rain forest in northern Suriname. 
Meded. bot. Lab. Herb. Rijks-Univ. Utrecht No. 163. 


80 Gardens’ Bulletin, Singapore — XX1X (1976) 


STAHL, E. 1896. Uber bunte Laubblatter, ein Beitrag zur Pflanzenbiologie. Annls 
Jard, bot. Buitenzorg 13: 137-216. 

STEENIS, C. G. G. J. van. 1942. Gregarious flowering of Strobilanthes 
(Acanthaceae) in Malaysia. Ann, R. bot. Gdn Calcutta, 150th Anniv. vol. 
pais. 7 

STRASBURGER, E. 1965. Textbook of Botany. New English ed. from 28th 
German ed, Trans. P. R. Bell & D. E. Coombe. Longmans, London. 


WALTER, H. 1971. Ecology of Tropical and Subtropical Vegetation. Trans. 


D. Mueller-Dombois. Oliver & Boyd, Edinburgh. 


Comparison of the Phytomass Structure of Equatorial “Rain-Forest” 
_in Central Amazonas, Brazil, and in Sarawak, Borneo 


by 


E. F. BRUNIG 
Chair of World Forestry, University of Hamburg 


H. KLINGE 


Max Planck Institute of Limnology, Department of Tropical Ecology, Ploen/ Holstein 


Introduction 


The ombrophilous predominantly evergreen lowland forests parts of Sarawak 
and Amazonia grow on very similar geologic formations, on similar soils and in a 
similar climate. The one author enumerated very intensively the phytomass 
structure on a 0.2 ha rectangular plot, 64 km from Manaus on the Itacoatiara road 
(Klinge and Rodrigues, 1971, 1973; Fittkau and Klinge, 1973; Klinge, 1972, 1973a; 
Klinge et al., 1973). The other author enumerated similarly, except without weighing 
phytomass, 55 rectangular 0.2 ha plots on a wide range of sites in Sarawak and 
Brunei, two 20 ha full enumerations on podzol soils on Tertiary and Quarternary 
parent materials respectively and a 0.04 ha plots random sampling of 60 plots on a 
Holocene terrace (Brunig, 1968, 1970, 1974). The purpose of the Amazonian project 
was the analysis of phytomass structure, of the Bornean study the analysis of diver- 
sity within and between stands and of the diversity/site interrelationship (Ashton 
and Brunig, 1975; Brunig, 1973a, b). General information on forest types, flora, and 
ecological conditions in the Amazonian area is given by Duke and Black (1953), 
and by Hueck (1966), in the Bornean area by Ashton (1964), Richards (1974) 
and Brunig (1975). 


In this paper the term ‘Central Amazonia’ and ‘Central Amazonian rain 
forest’ are used according to Fittkau (1969) who defines ‘Central Amazonia’ as 
a geochemical-ecological unit which is clearly distinguished from other parts of 
Amazonia. 


The Sample Stands 


The Amazonian plot is typical for mixed “terra firme’ forest on well drained 
loamy soils (Anon., 1969). Bleached sands and podzols occur in the neighbourhood 
at some distance but not in the plot area (Klinge, 1965, 1968, 1973b). Close to 
the plot were short steep slopes and alluvial valley bottom which carry different 
types of forest (Takeuchi, 1961). 


Plots were selected from the Bornean material to represent a wide range of 
site conditions and of stand structure, and also to indicate the size of within-stand 
variation of essential phytomass features against which the Amazonian plot could 
be assessed. The selected plots are briefly characterized in tab. 1. The plots selected 
from the 20 ha sampling area in Sabal Forest Reserve have not yet been fully 
analysed as they are intended for comparison with data from the San Carlos 
“MAB” project area, Amazonas, Venezuela, which is being enumerated in 
1975-1976. 


81 


d [cm] 


35 


30 


25 


20 


15 


@ 103 
bi 

7 138 
Lecythidaceae 

© 210 

@ 212 
Leguminosae coesaip, 

@ 233 

* 235 
Leguminosae 

@ 286 
Moraceae 

@ 323 
Myrtaceae 

@ 345 
Palmae 

a 381 
Rubiaceae 

a 416 


Sapotaceae 
@ 449 

Violacece 
e 490 
x 491 


40 hm) 


Fig. 1. Diameter — 
height correlation for 
representatives of 
plant families which 
according to theif 
number of species 
and/or individuals are 
the most important 
ones in the Central 
Amazonian rain forest 
(acc. to Klinge & 
Rodrigues). Top = 
whole stance, 
= enlarged for u 
growth. 


83 


Phytomass structure, equatorial rain forests 


uOIpIsSUeI] FOW/sesurloy 
UOI}ISURI] FOW /sesurloy 


sesuvloy 
sesuvloy 


UOIISURI] JO /sesurloy 
UOI}ISULI] FOW /sesurloy 
sesuvloy [e}SvOD 


sesuvloy [eIseog 


ysolOJ divoolojidiq poxify 
‘yedeloy ouvjuowqns 
sesurloy oueyUOUIqnS 
sesurloy suejuOWqns 


sesuevloy ouvjyuOWqnsS 


odA} 4S8010,7 


00S-9Lb 
SLv-ISP 


O0E-9L7 
SLC-1S7 


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84 Gardens’ Bulletin, Singapore — X XIX (1976) 


Forest Structure 


Stratification and stand height 


Our data indicate overlapping ranges of height in the various strata (tab. 2) 
and consequently indistinct storey formation of diameter/height relationships. The 
question whether tropical rain forest is stratified or not is controversial and views 
are conflicting (Rollet, 1973; Whitmore, 1975). While geometric stratification is 
often indistinct and obscure in mature stands on well-drained normal sites and 
soils, addition of floristic variation and plant geometry often produces more 
distinct layering in terms of overall diversity variation pattern. Distinct layering 
with discernible gaps between two or more layers is common on sites with 
extremes of environmental conditions or in some phases of development (Brunig, 
1970, 1975; Ashton and Brunig, 1975). For Amazonian rain forest Klinge and 
Rodrigues (1968), Aubréville (1961) and Soares (1957) describe the existence of 
storeys in general terms but the information is not supported by quantitative 
analysis. Maximum heights of 35 and 40 m are reported by Klinge and Rodrigues, 
Rodrigues, and by Takeuchi, and of 25 to 30 m by Aubréville, and Soares. 


The following general description of the stratification of the forest is mainly 
based on our own data, amended by data of the other authors: 


A-layer: a few very large trees overtowering the following 
B-layer: a non-continually, vertically ill-defined upper tree layer 


C,-layer: lower tree layer composed of mainly young or suppressed indivi- 
duals of species which are dominant in the upper tree layer. 
Occasionally, there are palm-trees. 


Almost all trees of the A-, B- and C,- layers show stem-rot increasing in 
severity from smaller to thicker stems. 


C,- and D-layers: a rather continual, vertically illdefined upper shrub layer 
with many saplings and with especially many acaulous palms. 


E-layer: dominated by acaulous palms and composed predominantly of 
saplings and seedlings; real herbs being scarce. 


All layers are heavily interlaced by lianes, many of which have thick stems. 
Vascular epiphytes are rare; there are some hemi-epiphytes, saprophytes, and 
parasites. Old palm fronds and old leaves of many tree species are heavily covered 
with algae and bryophytes. Crowns of the upper layer are up to 40 m wide; in the 
lower layers crowns have narrower conical forms. 


In comparison, Bornean forests on similar sites are taller, the A and B strata 
are more complex, and generally exhibit much diversity of structural characteristics 
in relation to site and phasic development. 


Number of trees 


The total number of trees, lianes, palms and herbs per unit area varies very 
widely in tropical moist forests as a result of differences in site, in stage of phasic 
development and spatial distribution pattern. In the Manaus plot the density per 
ha of all trees and palms above 20 cm height is 94,000 individuals (tab. 3). This 
agrees very well with the 73,000 trees and 6,000 palms recorded by Aubréville. 
Both figures do not include lianes, vascular epiphytes etc. Much lower figures for 
tree and palm density or total density were found by Takeuchi. Lechtaler’s figure 
745 stems (dbh 8 and more cm) agrees well that of Takeuchi. 


In the Bornean plots (nos. 43 to 53) the total number of trees > 2 cm d 
varies between 8028 and 12,133 per ha which indicates the scale of variation in 
number of trees which is of about the same order as the variation of basal area 
(35.3 to 50.9 m?/ha in the selected plots, sample mean of all 55 plots 36.5 m?/ha 
with a range of 27.0 to 88.0 m?2/ha). 


Phytomass structure, equatorial rain forests 85 


Table 2. Stratification of the Central Amazonian rain forest on level terra firme acc. to 
Klinge & Rodrigues (plot size 0.2 ha) 


Lower crown height 


| Upper crown height 
(m) 


(m) 


Stratum | Individuals 
ivy botkier ofl H.tisive bon per ha 
Mean Range | Mean Range 

A 35.40 38.10 — 32.10 | 23.70 29.00 — 20.00 50 
B 25.90 30.50 — 20.40 | 16.70 24.60 — 8.70 315 
=. 14.50 21.90 — 10.05 | 8.40 8.70 — 2.70 775 
ee 5.90 11.00 — 2.70 3.60 7.80 — 0.70 2,920 
D 3.00 4.50 — 1.55 1.70 2.90 — 0.20 6,070 
E 1.00 1.50 — 0.20 | 0.10 0.20 — 0.05 83,650 

93,780 


Bole diameters 


Height/breast-height diameter (h/d) ratios vary with species, site and age. 
Emergent trees frequently have ratios between 25 and 50, trees in the B-layer about 
50 and trees in the lower canopy between 60 and above 100. Ratios vary strongly 
even within one species in a stand and even more between species often obscuring 
any existing tendency to layer formation. 


Fig. 1 shows the relationship between total height and d for 14 plant families 
which according to numbers of species and/or individuals are the most important 
in the Manaus plot. The wide scatter in the taller strata is typical and agrees with 
observations in the Sarawak plots (Brunig, 1975, fig. 11d). 


Table 3. Plant density per height class and ha in the terra firme rain forest of Central 
Amazonian acc. to Aubréville (plot size 500 m2 (1) and 175 m2 (2), respectively) 


| | | 2 
Height class | 
(m) | 
| Trees Palms ! Trees Palms 
ae ia | 
> 15 | 340 60 | 514 0 
po. . 0S 300 20 | 629 57 
>? 2,940 1,560 | 3,714 1,143 
/ | 
Pach BE | 3,580 1,640 | 4,857 1,200 
x1 | ? ? | 68,229 5,029 
pak 
| 
Total — — 73,086 6,229 
Linas >I mi. 880 | 1,254 
simi, ? | 7,467 
Herbs <Imh_. v4 / 6,327 


| 
! 


Total | eas | 94.363 


86 Gardens’ Bulletin, Singapore — X XIX (1976) 


The ecological significance of stand curves (tree frequency distributions over 
d) in tropical forests has been recently reviewed by Rollet (1973). The shape of 
the stand curves is subject to many environmental influences and to intrinsic 
properties of the stand; variation between stands and sites, and within stands with 
time, is correspondingly large (Ashton and Brunig, 1975; Brunig, 1975). The 
Manaus plot shows a strongly truncated distribution, the largest diameter being 
only 55 cm, compared with a site related range of 50 to 100 cm in the 5 Bornean 
plots. 


Phytomass 


The phytomass data from the Manaus plot are the only available precise 
figures for the Amazonian lowland forest. The data are summarized in tab. 4. The 


Table 4. Fresh phytomass of the Central Amazonian rain forest acc, Klinge & Rodrigues 
(size of study plot 0.2 ha) 


Fraction Phytomass (t/ha) 

Trees and palms, A 190.2 
— above ground B 399.5 

Cc. 77.2 

C, 15.7 

D 4.7 

E 1.5 
— below ground 255 
Lianes, epiphytes, etc. 89 


Total | 1,033 


corresponding volume of tree boles in m3/ha is 385 > 15 cm d and 304 
> 25 cm d. These volumes and the corresponding fresh phytomass lie within the 
range of data reported by authors (tab. 5) and by the data of the FAO inventories 
south of the Amazon River. Compared with other tropical moist forests, the 
amount of stem volume and, consequently, of stem wood volume is rather low in 
the Central Amazonian rain forest. However, the terra firme forest of the Manaus 
area is not the most luxurious forest in Amazonia (Rodrigues, 1967). The total tree 


Table 5. Fresh phytomass of the Central Amazonian rain forest stands calculated under 
the assumption of a phytomass content equal to that in the Manaus plot. 


Fresh phytomass 


Authors (t/ha) Remarks 

Soares 360 Average of 2 surveys of 9 and 36 ha 
respectively . 

Rodrigues 413 Average of 27 ha 

Aubréville 510 Average of 2 surveys of 500 and 175 m2 
respectively 

Lechthaler 1,000 1 survey of | ha 

Klinge-Rodrigues 1,000 1 survey of 0.2 ha 

Takeuchi 1,350 0.16 ha section of 3 surveys comprising 
0.185 ha 

tne 
Mean 770 


Phytomass structure, equatorial rain forests 87 


volumes above ground estimated as V = G - 0.5 h (where G = basal area 
per diameter class, h = height of the diameter class) in the 55 sample plots in 
Borneo range between 195 and 1760 m3/ha. Determining factors are again site, 
developmental phase and the presence or absence of gregarious species which 
successfully reduce competitors on certain, often extreme and difficult sites. The 
mean value is 778 m3/ha (mean basal area 36.5 m*/ha of trees above 2 cm d). 
The fresh weight of phytomass is of the same order in t/ha as the volume 
estimator in m3/ha, and varies in the same range. The tree volumes naturally vary 
not only in relation to natural factors, but also to the size and shape of the plots. 
Variation increases as the size of the sample plots decreases, and deviations are 
less for transects than for squares. 


Maximum and minimum figures for total above-ground phytomass of living 
trees and palms in layers A-D were calculated for sub-plot sections which vary in 
size and shape (fig. 2). These figures indicate that sampling the phytomass distribu- 
tion of an area by transects apparently gives a better representation than by blocks. 
It can also be seen that the curves for maximum and minimum phytomass figures 
are not symmetrical. 


Fresh phytomass 
(metric t/ha) 


@ square plots 


© fectangular transects 


1,000 
500 
Extent 
of study plot 
0" 400 400 500 900 1,600 2,000 


Fig. 2. Maximum (upper curve) and minimum figures (lower curve) for fresh phytomass 
of layers A—D, calculated for square blocks and rectangular transects of different 
extent within the 0.2 ha plot of Klinge & Rodrigues, in the Central Amazonian rain 
forest. 


Assuming the above-ground living phytomass in layers A-D to be 68.7 % of 
the total living above-ground phytomass, the total living above-ground phytomass 
reported by Aubréville (0.05 ha plot) as 350 t/ha is less than the figure of 415 
t/ha which we obtain in a corresponding transect. Takeuchi’s 0.16 ha transect 
would include 927 t/ha which is more than the 710 t/ha we get in the Manaus 
plot for a square block of equal area. The figures of Lechthaler and Klinge & 
Rodrigues are identical despite the fact that Lechthaler’s plot is 5 times larger 
than Klinge & Rodrigues’ plot. Very low figures are obtained for the data of 
Rodrigues (27 transects of 1 ha each), and of Soares (9 and 36 transects, respecti- 
vely, of 1 ha each): 284 t/ha for Rodrigues’ plot, and 247 t/ha for Soares study. 


88 Gardens’ Bulletin, Singapore — X XIX (1976) | 


Number h >150em,d > Tem 
of species 


500 


0,1 0,5 area 1,0 ha 
d incm 

> 25 
735 
756 

300 
>15 

100 

Oj 9 27 36 


area in ha 


Fig. 3. Species number as a function of diameter class, size and shape of study plots in 
the Central Amazonian rain forest. 


Upper part: plots up to | ha in size. 
Lower part: plots up to 36 ha in size. 


89 


Phytomass structure, equatorial rain forests 


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90 Gardens’ Bulletin, Singapore — X XIX (1976) 


These low figures are possibly caused by site heterogeneity, The 5,000 m long 
transects of both authors in addition to latosol also included groundwater- 
influenced valley soils, bleached white sands and podzols, and flanks of valleys. 


Floristic structure 

Sample plots contain architectural and floristic variation of small-scale (tree 
groups in the order of 0.1 ha) and medium-scale (stands of 1 to several ha) 
(Brunig, 1975; Ashton and Brunig, 1975). Accordingly, in addition to the wide 
variation in architectural features (basal area, height, layering, diameter, frequency), 
there is considerable floristic variation (species complement and species dominance 
pattern, species for a number of reasons often occurring vicariously) between plots 
which is governed by chance the more the smaller the plot size. As a result, family, 
generic and species dominance figures for small plots are only meaningful if they 
are supported by data from larger-scale sampling of the wider surrounds on the 
same site types (Brunig, 1973). However, some features of floristic structure are 
somewhat more general and more consistent even in small plots, such as species- 
area and species-dominance curves. 


In the Manaus plot the 5 leading plant families Moraceae, Lauraceae, 
Leguminosae, Lecythidaceae and Sapotaceae on an average represent 50 to 60 % 
of all species, and 50 — 70 % of all individuals. Leguminosae and Lecythidaceae 
strongly exceed Lauraceae, Moraceae and Sapotaceae. The other authors for the 
reasons given above report different proportions and family dominances, e.g. in 
Takeuchi’s survey the Guttiferae are conspicuous, the Olacaceae in Lechthaler’s 
plot and Olacaceae and Euphorbiaceae in Rodrigues’ survey. 


Generally in Central Amazonia, second in number of species and/or indivi- 
duals are the Apocynaceae, Annonaceae, Rosaceae (Chrysobalanaceae), Bur- 
seraceae, Euphorbiaceae, Myrtaceae, Olacaceae, Celastraceae, Humiriaceae, and 
Myristicaceae. These 10 plant families on an average represent 20 — 40 % of the 
number of species and 20 — 50 % of the individuals. 


The group of rare plant families is the Guttiferae, Caryocaraceae, and 
Bombacaceae, and 40 plant families are very rare. 


Palms as a family are generally well represented. The acaulous species belong 
to the lower strata of the forest and are included only when the survey includes 
small sizes. A few palm species are cauliferous and intrude the middle forest 
layers; their heights may measure up to about 15 m. 


The Central Amazonian rain forest is composed of about 55 families and 
about 500 more common tree species (fig. 3). Rare species or families increase these 
figures for more extensive areas. Despite this high number of species and plant 
families, the Central Amazonian rain forest is poorer in species and less diverse 
than the Bornean Mixed Dipterocarp forest in Sarawak (Brunig, 1973a). 


Including small palms and woody species of low habit, herbs of the ground 
vegetation, and epiphytes, the total number of plant families in the Central 
Amazonian rain forest is supposed to be about 70, and its number of species 
about 700. There is no information on the number of cryptogam and vascular 
cryptogam species and families. The latter group is not well represented, but the 
cryptogams are very numerous, especially in the phyllosphere. 


We used data of the other authors for the construction of various species-area 
curves. The curves for the girth classes of 25, 35, and 56 cm rise steeply and 
smoothly (lower part of fig. 3). The curve for the next lower girth class (15 and 
more cm) is in its lower part above the curve of the 25 cm dbh class and its 
inclination is stronger. The curves for area below 1 ha are reproduced at larger 
scale in the upper part of fig. 3 which also includes the curve for dbh of 8 cm 


Phytomass structure, equatorial rain forests 91 


or 10 cm. It also includes >1 cm d or >150 cm h, which increase extremely 
rapidly to 0.2 ha and then flattens. It eventually would cross the curves for girth 
classes 25, 36 and 56 cm at plot sizes of 30 — 35 ha and species numbers of 
about 500. This agrees with the contention of Brunig (1968 and 1973a) that small 
plots cover the total species population satisfactorily, if very low diameter limits 
below or of 1 cm are adopted. Larger minimum sampling sizes require very much 
larger plot sizes if the less common and rare species should be adequately sampled. 
A diameter limit of 25 cm requires plot sizes of 30 and more ha. Intermediate 
diameter limits between 10 or 15 cm require about 15 to 20 ha, provided the 
forest and site are reasonably uniform. 


In the same sections of our 40 x 50 m plot, previously used for maximum and 
minimum phytomass calculations, maximum and minimum numbers of species 
were counted (tab. 6 and fig. 4). Differences between maximum and minimum 
species numbers are much smaller than the differences between maximum and 
minimum phytomass. The number of species is somewhat larger in transects than 
in blocks of similar size. 


n Species 
5 
e square plots 
© rectangular transects 
3 


Extent 
of study plot 


0 100 400 500 900 1,600 2,000 


Fig. 4. Species number as a function of plot size in the Central Amazonian rain forest acc. 
to Klinge & Rodrigues. 
Upper curve: maximum figures for species number. 
Lower curve: minimum figures for species number. 


The shape of species-areas curve is strongly influenced by site heterogeneity. 
In the Sabal sampling area, Sarawak, the increase of species number with transect 
length (20 x 500 m) is first steeper but then flatter in more xeric, oligotrophic and 
relatively homogeneous parts with tendency to single-species dominance (transect 
pairs 251-275 and 276-300 in fig. 5). It is first flatter but continues to rise steeper 
On more heterogeneous medium sites (1-25, 26/50), but again similar 
to the first pair on transitions to red latosols where again one species attains strong 
dominance (Dryobalanops beccarii Dyer). This is discussed in detail in an earlier 
paper (Brunig, 1973a). 


Floristic and phytomass structure 


The floristic and phytomass structure of a stand can simultaneously be 
expressed by the species-dominance curve. The curve for this purpose represents 
the contribution of each species to the stand basal area. The species are plotted 
in order of their contribution in percent of the stand total. The starting point of 
each curve is chosen arbitrarily so that crossing of the curves is avoided. One 
advantage of the species-dominance curve for putposes of comparison is that its 
significance is independent of the chances of species presence which is useful for 
small plots in floristically heteregeneous, diverse stands. The species-dominance 


92 Gardens’ Bulletin, Singapore — XX1X (1976) 


curves of a number of plots in different forest types in Sarawak (incl. sample plot 
43) is shown in fig. 6. The stands are arranged in order of improving site and soil 
conditions from the left (SP 40, Dacrydium pectinatum Delaubenf. bearing 
Kerangas on peat bog) to the right (SP 16, Dryobalanops beccarii bearing Mixed 
Dipterocarp forest). The dominance of the leading species is strong to the left 
(Shorea albida Sym, in SP 27 and Agathis dammara (Lamb.) L. C. Rich. in SP 
43) and weak to the left. Increasing flatness indicates that the mutual exclusion 
principle weakens and random distribution of ecological niches prevails. The 
species-dominance curve of the Manaus plot shows by comparison the least degree 
of species dominance and the flattest trend of the curve. This means that distribu- 
tion is largely governed by chance and more so than in the Bornean plots. This 
result cannot, however, be generalized because the Bornean plots, including SP 
16, are on less favourable soils than the terra firme plot at Manaus. 


Figures for both phytomass and species numbers in sections of different size 
and shape of the original 40 x 50 m plot were calculated separately for each layer 
as percentages of the figures for the total plot (fig. 7 — blocks; fig. 8 — transects). 
The minimum figures for phytomass and the corresponding numbers of species are 
shown in the upper part of both figures and the corresponding maxima and species 
numbers in the lower part. Figs 7 and 8 indicate that the lower forest layers 
represent a low proportion only of the phytomass, but a very large proportion of 
the total number of species. Therefore, the overall distribution of species within 
the plot is much more homogenous than the distribution of the phytomass. This 
observation agrees with the finding of Webb ef al. (1972) in the subtropical forest 
of eastern Australia. 


n species 
Species- Area Curve 


Sabal pm cai 
yr 1-25 
476-500 


100 — 
—_— 5 


Yj | aa oe 276 -300 
P< o 

y 

// 


0 5 10 15 20 25 
Number of chain-squares 


150 


50 


Fig. 5, Species-area lines for pairs of transects, each 20 x 500 m, in the Sabal sampling 
area, Sarawak. For plot description see tab. 1. 


93 


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94 Gardens’ Bulletin, Singapore — X XIX (1976) 


The inverse importance by phytomass and by number of species of the 
various size classes or stand strata is general for tropical moist forests. Fig. 9 
shows the same relationship for SP 43 as an example of a stand in which a single 
species attains extreme dominance, and fig. 10 for SP 53 with a more balanced 
floristic structure. The two samples again demonstrate the wide variation of 
structural parameters which exists in tropical moist forests. This is supported by the 
summaries of the cumulative species/size class and cumulative biomass/size class 


% 
100 


pe 

ss A 

oO e A 

eee species ; 
2a 
oO 


50 


biomass ~~ 


aD oe “"B 


eee ee ——— 


0 DO NG ae B A 


e square blocks, 40 x 40 m a 4 square blocks, 30 x 30 m © + square blocks, 10 x 10 m 


re 


biomass 
D C5 Cy B A 


Fig. 7. Increase of species number and phytomass of layers A-D in square blocks of different 
size, as per cent of the totals in the 40 x 50 m plot of Klinge & Rodrigues. The 
curves delimit the variability range of the figures. 

Above: minimum figures of phytomass and corresponding species numbers, and 
minimum species number and corresponding phytomass. 

Below: maximum figures of phytomass and corresponding figures of species number, 
and maximum species number and corresponding phytomass. 


Phytomass structure, equatorial rain forests 95 


curves for the 5 selected Bornean sample stands (fig. 11 and 12). These examples 
show clearly that efficient biomass sampling can be done with a relatively large 
minimum diameter limit which may be as high as 20 cm in stands such as in 
SP 43 or 10 cm in SP 53. But efficient sampling of species composition would 
require much lower minimum diameter limits close to zero. It was for this reason, 
that such low limits were chosen in the sampling of the 55 plots in Borneo which 
in fact covered an estimated 90.3 % of the species which are present in the associa- 
tion group of Kerangas and Kerapah forests (Brunig, 1973a, 1975). 


% 
100 


a en gn 


exo 


50 


fet 3 


D C5 C, 8 A 


——_——————— 
De 


= x rectangular transects, 40 x 10m @ 0 rectangular transects, 10 x 50 m 


% 


10 0 ——————— noe 
See oe ae 
n Species e 
° 
g 


8 
Biomass 
Sa iis et 


D Co C, 8 A 


Fig. 8. Increase of species number and phytomass of layers A-D in rectangular transects of 
different size and direction, as percent of the totals in the 40 x 50 m plot of Klinge 
& Rodrigues. 
The curves delimit the variability range of the figures. 
Above: minimum figures of phytomass and corresponding species number, and 
minimum species number and corresponding phytomass figures. 
Below: maximum phytomass figures and corresponding species number, and maximum 
species number and corresponding phytomass figures. 


96 Gardens’ Bulletin, Singapore — X XIX (1976) 


Table 7. Percentages of plant families on total numbers of species and individuals in 
the Central Amazonian rain forest acc. to Klinge & Rodrigues (dbh 15 and more cm) 
Lechthaler (dbh 16 and more cm), and Soares (dbh 15 and more cm) : 


Klinge & Rodrigues Lechthaler Soares(2) 
3 


Plant families (3) 
0.2 ha 1 ha 9 ha. 


Moraceae l. 
Lauraceae l. 
Leguminosae 20. 
Lecythidaceae S. 
Sapotaceae yA 


(6.5) 0.7 (17) 


(27.4) 14 (11.2) 
(11.6) 2.1 (9.4) 


2 ee 
——————— 


lst Subtotal 54.6 (44.3) 60.7 (69.7) 4.3 (22.3) 


Apocynaceae 3.6 5.4 ae 
Annonaceae 1.8 3.6 1.9 

Celastraceae 1.8 (1.4) 1.8 es M fi Cs 
Euphorbiaceae 10.9 1.8 ae 
Olacaceae 3.6 3.6 (4.7) o 


2nd Subtotal 21.8 (31.4) 161° AN 0.7 (1.9) 


Anacardiaceae 
Burseraceae 
Combretaceae 
Cucurbitaceae 
Flacourtiaceae 
Guttiferae 
Myristicaceae 
Rosaceae 
Rubiaceae 
Sapindaceae 
Simaroubaceae 


3.6 (8.4) 0.7 (7.7) 


RA 


0.7 (2.4) 


1.8 (2.3) 


x KKKXKXKXXKXXK X 


Vochysiaceae 
Violaceae 
Humiriaceae 
Icacinaceae 
Myristicaceae 
Caryocaraceae 
Nyctaginaceae 
Myrtaceae 
Bombacaceae 


(5.7) 
(4.3) 
(2.9) 


WW I 
N WW 


Reese 
a Rba2e 


| xxxxXx 


3rd Subtotal 23.6 (24.3) 


| 

N 
\o 
= 
oo 
SL 


Total 
n families 18 21 11 
N species 55 56 140 
n individuals 70 215 2250 


Palmae 


species l 
individuals 1 ; ‘ 


* 


Phytomass structure, equatorial rain forests 97 


Plot 43 
Fig 9 Sample Plo % Fig. 10 Sample Plot 53 


Species Species 


Biomass 


oe] 1 2 3 4 5 6 7 8 


10cm diameter Class 
10 diameter class 


Fig. 9. Cumulative relative species number and phytomass (biomass) with increasing diameter 
class in an Agathis dammara bearing Kerangas forest on Deep Humus Podzol, SP. 
43, Sarawak, 


Fig. 10. Cumulative relative species number and phytomass (biomass) with increasing 
diameter class in a mixed Kerangas forest on Grey-White Podzolic clay soil, SP. 53, 
Sarawak. 


"lg # BIOMASS 


Fig 12 Sample Plot 43,44,51,52,53 


Fig. 11 Sample Plot 43,44,51,52,53 


10-cm diameter class 


10cm diameter class 


Fig. 11. Cumulative relative species number with increasing diameter class in 5 selected 
sample plots, 0.2 ha each, in Sarawak. 


Fig. 12. Cumulative relative phytomass (biomass) with increasing diameter class in 5 selected 
sample plots, 0.2 ha each, in Sarawak. 


The variation of phytomass between 5 square 20 x 20 m subplots in the two 
sample plots SP 43 and SP 53 is illustrated in fig. 13 and fig. 14. The figures show 
Clearly the common feature: variation is much smaller in the lower size classes 
than in the larger size classes, but variation in the single-dominant stand 
(SP 43) is again less in the dominant emergent layer (71-80 cm d). It is interesting 
that the latter feature disappears again in the course of phasic development along 
a time-related ecological gradient which culminates in sample plot 44 (fig. 15). 
The strong dominance of A gathis dammara has weakened. The top canopy is more 
mixed, the stand structure more diverse and the stocking more variable between 
subplots. Obviously, such features have important significance not only for biomass 
and species sampling, but also for the structure and functioning of the ecosystem 
as a whole (Brunig, 1970, 1973b). 


Conclusion 


Available information on the Central Amazonian and Bornean rain forest 
permits the conclusion that relatively small plot sizes, such as the 40 x 50 m and 
20 x 100 m plots we used, have advantages for sampling both species composition 
and its phytomass. The small size is time and labour saving and cost-benefit 
efficient. Very large plots are proportionally costly and time consuming, and 
require an inordinate amount of facilities and organization because of the enormous 


BASAL AREA PER SQUARE AND 


OIAMETER CLASS 
G inm2 


S$P.63 
G inm? BASAL AREA PER SQUARE AND 
DIAMETER CLASS 
SP. 43 
$a. 6 
4 
3 
2 
1 
; 1SQ = 404.7 m? 
1 SQ = 404.7m2 
15 
1,0 
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Ry 
Ny 
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ne OO} (3 Cy 
SLA LX J is all 
O-6 6-10 11-20 21-30 31-40 41-50 51-60 «81-70 71-80 oe, 6 oe Os 8 68 ee ee 
Fig. 13. Basal area in m2 in each of the 5 Fig. 14. Basal area in m2? in each of the 
subplots (1 sq. ch.) of sample plot 5 subplots (1 sq. ch.) of sample 
SP. 43, Sarawak. plot SP. 53, Sarawak. 
G in m2 


BASAL AREA PER SQUARE AND 
DIAMETER CLASS 
2.5 SP. 44 


Fig. 15. Basal area in m2 in each of the 
5 sub-plots (1 sq. ch.) of 
sample plot SP. 44, Sarawak. 
The plot follows in a succes- 


1 SQ = 404.7 m2 


1,5 sion-related catena on SP. 43. 
The X — axis denotes diameter 
at breast height in cm. 

d in cm. 
(x) : KY 
a OM he OM 
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ma Pt ba MY 
VY) NY ws we x) 
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? 
; 
e 
3 
. 
8 
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8 
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Z 
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Phytomass structure, equatorial rain forests 99 


number of individuals and the greater number of species especially if site and 
forests are not homogeneous. However, if emphasis is on the rare or very rare 
species, plot sizes must be very large and diameter limits low. If only the forest 
phytomass is studied, small plots are adequate, especially with respect to the lower 
layers of the stand, and minimum diameter limits can be larger. The smaller 
material can be conveniently subsampled without much loss of precision. 


Our conclusion is in agreement with Lang et al. (1971) who studied tropical 
forest at Barro Colorado, Panama, and found that almost a 100 % sample is 
needed if the objective is to sample the rare species with high precision. The more 
common species are however adequately documented even if the sample comprises 
only a tiny portion of the total area. The examples from Borneo also confirm our 
earlier contention and Ashton’s (1964a) opinion that between-stand diversity and 
site diversity limit the useful size of vegetation sampling plots to around 0.2 to 0.5 
ha if within-plot homogeneity is desired. Expansion of plots beyond this size introdu- 
ces excessive heterogeneity by including different site and stand conditions. The 
variation of biomass parameters is of such magnitude and its pattern so complex 
that sampling of stand biomass and other structural stand features in natural 
virgin tropical rainforest must be done: 


by using small area plots if biomass is to be measured directly 


by rigorously stratifying the sampling design according to site conditions, 
phasic development and species composition 


——— by supplementing the biomass sampling in intensively studied plots by a 
survey of the wider plot surround with respect to the variations of biomass- 
related parameters such as basal area, stand height, tree shape, tree density, 
tree frequencies per diameter class and species composition. 


Unless these conditions are met, the results of studying small biomass 
sampling plots, as of other types of yield observation plots, will produce meaning- 
less, because uncoordinated, information. 


Acknowledgments 


Thanks are due to W. A. Rodrigues, Botany Department, Instituto Nacional 
de Pesquisas da Amazonia, Manaus, Amazonas, Brazil, who made some of his 
staff available for the fieldwork from June to November 1970, and who also helped 
in many other ways. 

The Amazonian data have been obtained through cooperation between the 
INPA, Manaus, and the Department of Tropical Ecology, M.P.I., Ploen. The 
Bornean data have been processed with financial assistance from the German 
Research Foundation. (DFG). 


Literature 


ANON. 1969. Os solos da area Manaus — Itacoariara. IPEAN, Série Estudos e 
Ensaios 1, Manaus, 116 pp. 


ASHTON, P. S. 1964a. A quantitative phytosociological technique applied to 
tropical mixed rainforest. Malay. Forester 27 (3): 304-317. 


1964b. Ecological studies in the Mixed Dipterocarp Forest of 
Brunei State. Oxford Forestry Memoir 25, Oxford. 


— and BRUNIG, E. F. 1975. The variation of tropical moist forests in 
relation to environmental factors as key to ecologically oriented land-use 
planning. Mitt. BundForsch-Inst. Forst-u. Holzw. 109: 59-86. 


100 Gardens’ Bulletin, Singapore — XX1X (1976) 


AUBREVILLE, A. 1961. Etude écologique des principales formations végétales 
du Brésil et contribution 4 la connaissance des foréts de l’Amazonie brési- 
lienne. Centre Technique Forestier Tropical, Nogent-sur-Marne, 268 pp. 


BRUNIG, E. F. 1968a. Some observations on the status of heath forests in 
Sarawak and Brunei. Proceedings, Symp. on Recent Advances in Tropical 
Ecology, Varanasi, 1967. Int. Soc. Trop. Ecol., Varanasi: 451-457. 


1968b. Der Heidewald von Sarawak und Brunei. Mitt. Bund. 
Forsch-Anst. Forst- u. Holzw. Nr. 68, Bd. I u. If, 431 pp. 


1970. Stand structure, physiognomy and environmental factors in 
some lowland forests in Sarawak. Trop. Ecol. 11 (1) 26-43. 


1973a. Species richness and stand diversity in relation to site and 
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1973b. Biomass diversity and biomass sampling in tropical rain 
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1975. Ecological studies in the Kerangas forests of Sarawak and 
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DUCKE, A., and BLACK, G. A. 1953. Phytogeographical notes on the Brazilian 
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FITTKAU, E. J. 1969. The fauna of South America. In: E. J. Fittkau, J. Illies, 
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HUECK, K. 1966. Die Walder Siidamerikas. Fischer, Jena, 422 pp. 
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1972. Biomasa y materia organica del suelo en el ecosistema de la 
pluviselva centro-amazonica. Acta cient. Venez. 24: 174-181. 


1973a. Struktur und Artenreichtum dez zentralamazonischen 
Regenwaldes. Amazoniana 4 (3): 283-292. 


1973b. Root mass estimation in lowland tropical rain forests of 
Central Amazonia, Brasil. I, Trop. Ecol. 14: 29-38; II. Anais Acad. bras. 
cienc. (1975, in press). 


KLINGE, H., and FITTKAU, E. J. 1972. Filterfunktionen im Okosystem des 
zentralamazonischen Regenwaldes. Mitt. deutsch. bodenk. Ges., Gottingen. 
16: 130-135. 


KLINGE, H., and RODRIGUES, W. A. 1968. Litter production in an area of 
Amazonian terra firme forest. Part I, Litter-fall, organic carbon and total 
nitrogen contents of litter. Amazoniana 1 (4): 287-302. 


1971. Matéria organica e nutrientes na mata de terra firme perto de 
Manaus. Acta amazon., Manaus 1 (1): 69-72. 


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Phytomass structure, equatorial rain forests 101 


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1973. Biomass and structure in a Central Amazonian rain forest. In: Ecological 
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LANG, G. E., KNIGHT, D. H., and ANDERSON, D. A. 1971. Sampling the density 
of tree species with quadrats in a species-rich tropical forest. Forest Sci. 
17: 395-400. 


LECHTHALER, R. 1956. Inventario das arvores de um hectare de terra firme 
da zona Reserva Florestal Ducke, Municipio de Manaus. Inst. Bras. Biblio- 
grafia e Documentacdo, Rio de Jan. Botanica, Publ. 3, 7 pp. 


RICHARDS, P. W. 1974. The tropical rain forest. 5th Ed. Cambridge Univ. Press. 


RODRIGUES, W. A. 1967. Inventario florestal pil6to ao longo da estrada Manaus 
— Itacoatiara, Estado do Amazonas: Dados preliminares. Atas Simpdsio 
sdbre a Biota Amaz6énica, Belém 1966, 7: 257-267. 


ROLLET, B. 1973. L’architecture des foréts denses humides sempervirentes de 
plaine. Centre Techn. For. Trop., Nogent sur Marne, 298 pp. 


SOARES, R. O. 1957. Inventario florestal Reserva Florestal Ducke. Relatorio. 
Mimeogr., 26 pp. 


TAKEUCHI, M. 1961. The structure of the Amazonian vegetation. II. Tropical 
rain forest. J. Fac. Sci. Tokyo Univ. Sect. 3, Bot., 8 (1/3): 1-26. 


WEBB, L. J., TRACEY, J. G. and WILLIAMS, W. T. 1972. Regeneration and 
pattern in the subtropical rain forest. J. Ecol. 60 (3): 675-695. 


WHITMORE, T. C. 1975. Tropical rain forests of the Far East. Clarendon Press, 
Oxford, 282 pp. 


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Autonomous Evolution in Plants 
Differences in plant and animal evolution 
by 
C.G.G.J. VAN STEENIS 


Rijksherbarium Leiden 


CONTENTS 
Page 
Summary - - - - - - : - - 103 
1. Introduction . - - - - - - - - 104 
2. Survival level and patio ludens - - . - - - : 107 
Anatomical features and structural fitness of Gymnosperms - - 109 
3. Pre-adaptations in plants - - - . . - - 111 
4. Early differentiation - - - - - - - - 112 
5. Saltatory evolution in plants - . - - - - - 113 
6. Gliding evolution in animals - - - - - - - 117 
7. Co-evolution of animals and plants” - - - - - - 119 
Evolution of orchids - - . - : - : - 121 
Evolution of figs’ - - - - - - - - 122 
8. Reticulate phylogeny - - - : - - - - 123 
9. Embryology and ontogeny” - - - - - - - 124 
References - - - - - - . - - 125 

Summary 


It is argued that after ’decisions’ were made in the early stages about the basic matrix of 
plant life later evolution followed in an autonomous way, not as a consequence of the 
competition /selection principle. 


Evolution of plants is characterized by their passive tolerance and lack of active aggres- 
sion. Their main struggle is to evolve against the environment; mutual competition is no 
agency for their evolution. Animal evolution has, besides this same struggle, a second 
impetus by competition. 


_ Under this dual pressure animal evolution is proceeding more rapidly and form-making 
is more abundant, and has led to more complicated specialized structural and behavioural 
development than in plants because of sexual selection, which is absent in plants. 


_ Competition and survival of plants is more passive and mainly directed against the 
inanimate environment. This tolerance led to a slower and conservative evolution. 


The survival level, which tops all requirements necessary for survival for a certain place 
and time, lies much lower in plants than in animals and allows for plants a greater free 
space (‘patio ludens’) for structural development of non-adaptive characters, which fall beyond 
competition, selection, and adaptation. This free space in animal development is generally 
considered to be very narrow. 


So-called ‘pre-adaptations’ in plants have not come into existence because of competition 
pressure, and is a misleading term in evolutionary sense. 


In early differentiation structural decisions for later phyla may well have been made by 
chance, or these characters may have had in those early stages a lower ‘genetical weight’ 
than they got during later establishment. 


In ‘plants, the usual way of evolving evolutionary development is through sudden 
(saltatory) change which is amongst others proved by preponderance of allopolyploid and 
aneuploid chromosome numbers. 


This saltatory evolution proceeded through a small number of specimens. 


103 


104 Gardens’ Bulletin, Singapore — XX1X (1976) 


Saltatory development may also have occurred through sudden change of a few genes 
which physiologically upset pathways to morphogenesis, partly through neoteny, and gave 
rise to systematical teratologies, and thus to creation of isolated taxa. 


Racial segregation may have led to new species but in plants only in exceptional cases 
(in long isolation): the term micro-evolution used for this development should be abandoned 
for plants. 


It seems not possible as yet to translate structural changes in genetical terms and define 
the constancy in genetical weight of genome structure, though there must be a considerable 
genetical difference between characters common to phyla and those common to families, 
genera and species. It is peculiar that by a sudden saltation of a ‘physiological gene’ a very 
constant structure may be upset, for example by a peloric form in an orchid. 


In animals on the other hand ‘gliding evolution’ by gradual accumulation seems to be 
the usual way of development. This is attributed to competition and sexual selection, and 
it goes by populations, through convivia, commiscua and comparia. 


Mutations irrelevant to divergent survival may be possible but they will play a minor 
role, as patio ludens is for animals a very narrow measure. Saltations, if they occur, must 
be quite exceptional. 


Co-evolution of plants and animals is usually a one-sided affair, in which changes in plant 
structure occur first, and adaptation by animals follows. Except for negligible exceptions 
plant evolution goes independent of animal evolution in an autonomous way; novelties 
arising in plants are exploited by animals for their evolution and specialization. 


This does not exclude that in a restricted number of cases plants got into a situation 
where animal action became a vital factor for their survival, as in orchids and figs. In these 
cases animal populations have forced their way of gliding evolution on that of plants, but 
even in these cases changes of plant structure do not arise perforce of competition among the 
plants themselves. their changes remain autonomous, it is the animals which adapt themselves. 


It is argued that, whereas in the gliding, divergent evolution of animals there will be 
hardly any chance of reticulate phylogeny, though their will be of course reticulate affinity. 


In plants, however, it has been shown that reticulate phylogeny has played an important 
role in their evolution. 


Finally attention is given to the basic difference between animals and plants in their 
embryological and ontogenetical development which must have had essential implications 
for their evolution. 


1. Introduction 


It is, I believe, generally accepted that evolution in plants and animals is 
caused by similar impulses and that its mechanism(s) has been the same for both. 
It should be remarked that this holistic principle is philosophically an extremely 
attractive axiom. It should, however, also be remarked that the development of 
evolutionary theory has largely been in the hands of zoologists and zoo-palaeon- 
tologists. They had of course no reason to check whether the axiom is fully valid 
for plants or whether there are differences, either in degree or in quality. 


From the side of botanists there have been, as far as I can remember, 
remarkable few queries about the validity of the holistic axiom. And those I know 
of concern only the proportional speed of evolution. 


J. D. Hooker (1859: xii, footnote) pointed to the marked contrast of the 
showy, vivid differentiation of the fauna as compared with the conservative, rather 
monotonous development of the plant kingdom, writing: “the much narrower 
delimitation in area of animals than plants, and greater restriction of Faunas than 
Floras, should lead us to anticipate that plant types are, geologically speaking, 
more ancient and permanent than the higher animal types are, and so I believe 
them to be, and I would extend the doctrine even to plants of highly complex 
structure’. The idea that changes in the development of the Angiosperms have 
been extremely slow was also stressed by Hamshaw Thomas (1961: 3). 


It appears in fact, that certain types of life, especially among the bacteria and 
algae, have persisted over immense periods, some two, or at least one and a half 
billion years, before showing further evolutionary development. 


Autonomous Evolution 105 


It is true that this observation relates only to the quantative aspect, the speed 
of evolutionary progress, but it leads nevertheless to consider the qualitative 
aspect, even if this would mean a re-appraisal of the holistic principle. 

Therefore we have to consider the mechanism(s) of evolution gradually 
developed through the ideas of Buffon c.s., Lamarck, Hutton, Malthus, Lyell, and 
finally synthesized by Darwin & Wallace, by whom the gradually grown idea of 
adaptation was more closely defined as adaptation caused by selection on the basis 
of competition, more popularly explained as survival of the fittest. 


Competition, resulting in selection, must of course have been a powerful agent 
through the history of life. It is supposed to have been already present on the 
abiotic level. Probably already at this stage was it effective, with the understanding 
that ‘decisions’ were made resulting in a restricted number of initial organic 
compounds (see Quispel, 1968). The same principle of competition is held res- 
ponsible for the evolution at the akaryotic and later karyotic stages at the biotic 
level. It is clear that competition results in restriction of the pre-existing variability, 
either by adapting the mechanism of segregation or by preferential elimination of 
less adapted individuals. 


In these early stages, again, ‘decisions’ were made about basic features of 
structure which became the matrix of later evolution. One may well imagine that, 
if ‘decisions’ had materialized in different ways, other matrix structures would have 
originated. Thus, the impact of these early competitions must have contained a 
very important factor of chance. Chance is in this context of course to be under- 
stood as causal, but it includes the possibility that matrix structures of genomes 
could have been different. The early ‘decisions’ made, must thus have had a 
decisive, hence restrictive influence on later evolutionary lines for further develop- 
ment. Once a stable basic matrix pattern of genome design was established, the 
fate of further evolution based on this design was curbed, the stakes of its 
potential boundary being set out, comparable to ‘evolution’ of basic designs in 
industrial tool and machine development. 


This implies that only part of the potentially possible organic structures really 
have got into actual existence as viable living organisms. We cannot fathom what 
other basic designs could have had viability, and so, questioning what percentage 
of the total potentiality of living matter was ever realized, becomes an impossible 
and useless exercise. 


The main basic design for plant evolution must have been the unicellular 
algae and bacteria*, probably soon followed by fungi. They must have been 
capable of conquering the earth, as they still do. They coupled plasticity against 
environmental factors with diversification, resulting in the occupation of all niches, 
as they still do. This diversification consisted of the origin of species adapted to the 
environmental niches of an unimaginable variety: freshwater, seawater to brine, 
arctic to tropical conditions, rock faces and snow, even extremely high water 
temperatures. It seems doubtful whether this can be explained or that it needs to 
be explained by the competition/selection axiom; the world was bare and niches 
unoccupied, it was free for all. 


Our unique planet once occupied by bacteria and algae, we are confronted 
with the question why there was any ecological or adaptational need or necessity 
for evolution to more complicated organisms according to the competition/ 
selection axiom as the mechanism of evolution. 


*I have always been surprised that virus is usually advanced as more primitive living matter, 
due to a more simple design. Since virus is inert matter, only capable of multiplication as 
a parasite in the protoplasm of more complicated real organisms, they cannot have preceded, 
or be ancestral to, the latter. 


106 Gardens’ Bulletin, Singapore — X XIX (1976) 


It is likely that the unicells were followed by thread-like, branched and 
foliar algae, which also needed space. They may have locally shaded out, but not 
replaced all the unicells. They were received as affiliated newcomers, to belong 
to one happy family. Under favourable environmental conditions there is no end 
to the extension of the family, as is e.g. shown by the tropical rainforest, the flora 
of the Cape or of New Caledonia or Western Australia which are not only very 
rich, but where also each family and each genus is represented by many species 
thriving peacefully together. | 


Here we glimpse a first difference, the passive tolerance of plants as compared 
with animals. Plants are tolerant living beings, they do not eat their close allies, 
they do not hunt and kill in order to survive, they do not need all sorts of devices 
towards upmanship in order to live. This passive tolerance, lack of active aggres- 
sion, suffering in silence, subdued happy-go-lucky mode of living, just waiting what 
will happen, this inertia as compared with animals, is characteristic of plants. To 
no mean degree this is due to the sedentary bond with the terrestrial substratum. 


Animals show generally motility, they show aggression, they are out to 
exterminate rivals, show competition and intolerance, and are for a great deal 
not sedentary and bound to the substratum, but move around. It should be 
mentioned that among the most highly evolved animals, viz. birds and mammals, 
there are striking examples of tolerance within the species, mutual aid, and even 
birth control by various sophisticated devices. Still, these are exceptions, and 
especially tolerance towards the members of other species is very rare. 


These two opposite tendencies, passivity and activity, must, I believe, have 
the important corollary, that animals are under greater pressure to develop steadily 
more complicated means and ways, including structures in order to keep up with 
competition and have to use all possible advantages, which by mutation occur, in 
order to survive. Their structure becomes in this way adapted to competition, 
leaving hardly room for organs or other features which are useless or irrelevant 
to survival. Their organization is thus changing rather rapidly; organs once useful 
have been superseded by others and though they often do not disappear entirely, 
they soon are hidden away and can only by careful comparative anatomy be traced 
as insignificant vestiges. 


Thus I believe that, while the competition/selection axiom is valid for animal 
life, plants behave more conservatively, as they do not suffer from similar pressure. 
They develop more slowly and give free way to inventiveness in forms and struc- 
tures which are irrelevant to competition/selection, creating features which some- 
times are called adaptively-neutral. 


It should be noted of course, that rudimentation in flowering plants, due to 
saprophytism, parasitism, or secondary aquatic life, is comparable to rudimentation 
in animals. Nevertheless, it seems to be less stringent in general, and it seems to 
proceed much more slowly. 


Competition and survival in plants is passive; it is mainly caused by or 
directed against the inanimate environment, heat and cold, drought and water, 
seasonal desiccation, exceptional soil types, and presence of toxic minerals, etc. A 
few exceptional cases of allelopathic behaviour mean only that certain plants may 
not tolerate others in their immediate vicinity, but there is plenty of room for them 
elsewhere. Besides, allelopathy does not concern competition between allied species, 
but rather implies an influence of exudates of non-related species. Parasitic plants 
may destroy or harm their hosts, but they usually come to a balance agreeable 
to the survival of both host and parasite, sometimes even to a parasitical symbiosis _ 
(Rafflesia, Balanophora, etc.). In their strife for light plants may shade out others, _ 
but there are always open places where the shade-giving plants cannot thrive and 4 
have to give way to the smaller ones. 


Autonomous Evolution 107 


There is no case known to me that a so-called better adapted plant completely 
outrooted another allied species. It has been shown that seedlings of one species 
may have an advantage over those of an other in experiments, but I doubt whether 
these experimental conditions can be applied to germination in nature, and if it 
were so, in nature it will always turn out to be a mere question of proportional 
abundance, not of extinction through competition. This can hardly be otherwise, as 
each plant species has its own ecology, including resulting abundance: no two 
species have exactly the same ecology. To be precise, and to quote a simple 
example: very few closely allied species of plants will be able to survive in a peat 
bog of high acidity, or in soils loaded with heavy metal ions, but we never observe 
that one species eliminates all others. 


In conclusion, it appears that intra- and inter-specific competition as well as 
natural selection (in the sense of elimination of weak individuals by stronger ones) 
among plants is insignificant. The occurrence and abundance of plants is almost 
entirely defined by environmental factors. 


Against animals in search for food, the plants behave passively. Many may 
contain poisonous substances, or elaborate structural devices which seem to be 
effective in keeping off some of the potential predators, but even in these cases 
it is the animals which adapt themselves; as a matter of fact the most toxic plants 
have animals which feed on them. Thus, it is essentially a question of equilibrium, 
based on mutual adaptation. 


Animals on the other hand have the problem of surviving two kinds of 
struggle for life. The first struggle is the same as that of plants, against the 
inanimate environment, but the second is against each other. Instead of the basic 
autotrophy of plants there is a food chain in animals, often very complicated, in 
which besides plants other animals take part. This dual struggle means a high 
degree of competition among animals, and thus a much higher pressure towards 
upmanship. This must inevitably lead to more rapid change and development, that 
is, evolution. 


A third point is that the number of niches for animals is much greater than 
for plants, and far more finely knit, enabling them to develop through the pressure 
of competition/selection an immensely greater display of form-development and 
specializations. 

A fourth, though minor, point is that animals can occupy certain environments 
unfit for plants, such as the depths of the oceans, the atmosphere, caves, etc. 


Concluding, this concise discussion may serve to explain the observation 
Hooker made, that the variety in the animal kingdom is far greater than that in 
the plant kingdom. 


What is more important, it throws also doubt on the holistic view of evolution 
in animate nature, in particular on the intensity of competition in the struggle for 
survival. 


2. Survival level and Patio Ludens 


The views exposed in the introduction lead to certain consequences which I 
have alluded to in my essay on plant speciation in Malesia (1969), viz. that there 
is a difference in the situation of the survival level in plants as compared with 
animals. I have illustrated this in a generalized schematic figure (Fig. 1). 


108 Gardens’ Bulletin, Singapore — XX1X (1976) 


Plants 


Patio ludens 


Fig. 1. For explanation see the text. 


The rectangles represent the total potential space for structural development, 
in conjunction with the degree of the minimum requirements necessary for survival. 
indicated by the hatched space. The demarcation is marked by a line, which I call 
the ‘survival level’; beneath it one has to think of all structures and functions 
compulsory for survival. 


Above the survival level there is ‘patio ludens’, represented by the blank space 
which can be occupied — but will not always be necessarily fully occupied — by 
structures which are irrelevant to survival, hence fall beyond competition, selection, 
and adaptation. 

Through the more intense competition and more complicated life of animals, 
I believe that patio ludens is for animal life only a narrow zone as structural 
development is under high pressure of competition/selection, and development is 
more acutely directed towards trying to employ and adapt any new feature which 
it can use for its survival. The survival level in animals lies thus considerably 
higher. It should be admitted though, that adaptive-neutral features have occurred 
in animals as well, at very primitive levels, e.g. when the divergence started in 
arthropods into the insect and arachnid phyla, but also at the level of speciation, 
as exemplified e.g. by protuberances (often allometric in behaviour) in protozoans, 
arthropods, vertebrates, etc. See p. 112. Also I would not exclude the possibility 
of a lower survival level in primitive groups of animals. 


In plants the survival level must generally lie much lower and primary struc- 
ture equipment is more primitive. There is no such competitional strife in perfection 
of adaptive structures as among animals. Consequently there is ample allowance 
for the possibility of structural features (form development) which are irrelevant 
to competition and adaptation. 


These irrelevant or adaptatively neutral characters in plants concern both 
gross morphological characters and internal characters. It is for a woody plant 
not a matter of competition whether it develops into a tree or liana or a scrambler; 
or whether a liana twines to the right or to the left. Phyllotaxis seems also a quite 
irrelevant character, all types are equally well fit to let a plant live and survive. 
Presence or absence of stipules can equally not be attributed to have special 
function for survival. To prevent any misunderstanding: functional adaptations are 
very important, but they are not in any way restricted by neutral basic features 
like e.g. phyllotaxis. 


Merousness of flowers also seems a matter of chance choice. Thus it would 
be a far-fetched idea to postulate that 5- or 4-merous flowers have a competitive 
value, the one better than the other, or 3-merous ones over 2-merous flowers (cf. 
also Bateson, 1894: 67). Monocotyledons are characterized by 3-merous flowers, 
but 2-merous ones do equally well (Stemona, Paris, etc.). 


Autonomous Evolution 109 


In the flower the number and position of anthers, obdiplostemony, etc. is an 
often systematically very constant structure, but it seems futile to ascribe com- 
petition value to such structures. In a very uniform genus, such as Tristania, the 
number ranges from 5 to very many (and then in phalanges); in Borneo many 
species grow together and none of them is crowding out the others. 


As to gynoecium, its position: superior or inferior, its merousness, the position 
of ovules, erect or pendent, axial or parietal, seems not to have any bearing on 
competition. It just happens that in families like Theaceae one or a few have by 
exception an inferior ovary (Anneslea) and in Rubiaceae some have a superior 
ovary (Gaertnera). Or this may vary even within one genus (Mastixiodendron). 
A similar situation prevails with the seed. It could not be argued with good reason 
that the presence of two cotyledons would be of any competitive value above the 
presence of one cotyledon, or for that matter of more than two. The same holds 
for the place where reserve food is stored, in the cotyledons or in albumen, or in 
both, or whether seeds are large or small. They all come up equally well ecologic- 
ally. As a matter of fact any systematic structure (systematic character) may be 
constant in one group and vary in an other; properly none of them have absolute 
value. 


In this context it is noteworthy what A. C. Smith remarked, when he spoke 
of the phylogenetic systematy of the Monimiaceae (1973: 55): “The basic 
complex with which we are here concerned, within the Ranales, is characterized 
by having comparatively primitive xylem, ethereal oil cells, monocolpate pollen 
or pollen derived from that type, and unilacunar nodes. Incidentally, these are not 
glaringly apparent characters, but they are some of the basic characters that 
taxonomists concerned with Angiosperm evolution must use if they seek to 
understand (phylogenetic) relationships”’. 


In all these structures plants do not compete, their only concern is to stand 
certain primary minimum conditions under the survival level. 


_ Concluding, it must be well understood as a major point that it is precisely 
these ‘technical characters’ which serve for the schemes of the evolutionary 
system of the Angiosperms, that is, that they reflect phylogenetic affinity and are 
employed for the reconstruction of their ancestral relations and derivation. Though 
these structures have no adaptive value, the way of evolution is traced by them. 
And this shows their importance. 


Anatomical features and structural fitness of Gymnosperms 


Even for anatomical features the evidence that complicated, specialized 
structures would have originated as a result of competition/selection to enhance 
their functional value, is dubious, if we try to measure their success. 


One might imagine that vessels for transport of water, assimilates and minerals 
would mean a great advantage over tracheids. This rough assumption is, however, 
not borne out by the facts, as among both groups are the highest trees known to 
exist, and the oldest in life-span are even among those without vessels. Furthermore, 
it is not so that among the vesselless trees growth need to be hampered by 
absence of vessels and thus growth would be slower. Saplings of certain conifers 
may show a very rapid upgrowth indeed, comparing favourably with that in 
eucalypts. Conversely it is not so that saplings or trees with vessels always show 
a rapid upgrowth; some grow extremely slowly. This whole matter is dependent on 
several factors, sometimes individually on soil and climate conditions, and 
Structure and capacity of root system, but mainly on the ecological capacity of the 
different tree species of each group, irrelevant of presence or absence of vessels. 


110 Gardens’ Bulletin, Singapore — XX1X (1976) 


A conclusion is sometimes made about the better adaptation by presence of 
vessels with reference to the palaeontological experience that Gymnosperms have 
very gradually been partly replaced by Angiosperms, in the sense that terrestrial 
space now occupied by Angiosperms was in pre-Cretaceous time the domain of 
Gymnosperms. This is certainly true, but it is doubtful whether this generality 
can be explained by improved ‘adaptive values’. On the one hand it should be 
remarked that anatomically and functionally the Jurassic Ginkgo was obviously 
a success, but similar things can be said of Araucaria, Metasequoia, Cycadaceae, 
and others. On the other hand trees equipped with Angiosperm-type wood 
from the Cretaceous had also to make place for newcomers. In addition it should 
be remarked that anatomists tell us that various anatomical features seem to be 
without function. Finally, the ‘decline’ of Gymnosperms is, I feel, slightly 
exaggerated; they are still responsible for a high percentage of all organic matter 
produced on our globe. This idea of ‘decline’ may, possibly in part be due to the 
proportionally low form-development which is indeed negligible if compared with 
the enormous diversity in structural development of Angiosperms. 

But this is altogether another matter than inadequacy or deficiency of 
structural and functional fitness. This matter belongs to the question one can also 
put for structural development of many phyla and groups: why some are ancient 
but remained small and others grew to great diversified groups. Even in the 
Mezozoic the Gymnosperms as to number of genera and species were probably 
always fewer in number than the Angiosperms are today. The only guess one can 
make in this obscure field of speculation is that the basic genome pattern of groups 
remaining small was ‘rigid’ and did not allow for abundant form-development, and 
that the genome pattern of so-called more successful groups or phyla was more 
suitable or ‘versatile’ and had the promise of more potentialities. Similarly as in 
chemistry certain atoms (for example C, Si, etc.) have more potentialities as the 
basis of compounds than others: or in terms of plants, certain species appear to 
be fit to be ‘developed’ into a large number of edible or ornamental variations, 
while others simply resist this and do not possess genome potentialities fit to be 
exploited by domestication. 

In chemistry potentialities of chemical evolution — in the sense of capacity 
of producing compounds — can be foretold. This should then also be possible for 
the chemical compound named genome-structure. But this is so complicated that it 
will never be possible to compute why the pattern in the Linaceous genus 
Ctenolophon, which existed already in the Upper Cretaceous, persisted all the time 
in the tropical forests (now extinct in the neotropics) but produced at most three 
species, while the obviously much later evolved Compositae, Acanthaceae, etc. 
showed an astounding diversification though they are structurally very homogeneous 
from the taxonomic point of view. 

I may mention a few other examples of old genera which are known from the 
Upper Cretaceous or Palaeocene which have never evolved into large groups, e.g. 
Pachysandra, Nypa, Knightia, and Gingko; contrasting these with Ilex, Quercus, 
Nothofagus, Alnus, Symplocos, etc., we cannot account for the latter’s successful - 
development, taxonomically and geographically, \: 

I do not believe that it will ever be possible to compute the causality 
structural development or account for the potentialities of the genome matrices an 
show that it could not have been otherwise and could be foreseen, or at leas 
expected. 


Autonomous Evolution 111 


I have stressed (1969) that a congenial, equable climate, such as the tropical 
rain forest, which has persisted ecologically unhampered for aeons, has the lowest 
competition pressure, hence the lowest survival level in all habitats for plants, hence 
for them the widest patio ludens. Consequently the tropical rain forest offered the 
longest and largest opportunity towards form creation on the globe, for all kinds 
of structural developments which came up to survival conditions. It became the 
cradle of the development of Angiosperms as well as many other groups of the 
plant kingdom. This is also the reason why the tropical flora contains so many 
isolated genera and, besides, the frame-work of all larger families, which swarmed 
out later to other parts of the globe. 


3. Pre-adaptations in plants 


This term has sometimes been loosely applied in an evolutionary sense, to 
explain for example the structure of seeds and fruits on the sandy beach. 


These fruits and/or seeds, which are all provided with some buoyancy device, 
are either hard-shelled, or have their seed surrounded by a stone and/or fibrous 
tissue and thus protected against the surf and grinding on sand, rock, coral and 
pebbles. But it must be kept in view that the representatives of the beach and the 
tropical beach-forest are just single or very few beach-specialized species of large 
inland genera which all display the same fruit-seed structure in inland 
vegetation, whether it be the hard-shelled Leguminosae (Caesalpinia, Canavalia, 
Desmodium, Erythrina, Pongamia, Sophora) or species of for instance the genera 
Barringtonia, Calophyllum, Casuarina, Clerodendrum, Colubrina, Cordia, Cycas, 
Cyperus, Dodonaea, Euphorbia, Fimbristylis, Guettarda, Hernandia, Hibiscus, 
Ipomoea, Ischaemum, Morinda, Pandanus, Scaevola, Spilanthes, Terminalia, 
Tournefortia, Wedelia, etc. 

To bring their morphological capacities in conjunction with adaptation, as 
so-called ‘pre-adaptation’, seems to me a serious misleading of evolutionary 
thought, as it suggests the childish idea of pre-sighting on the part of the plants 
that it might be useful to develop such structures, just in case it might be helpful 
to cope with the exigency of sharing the future life of a beach-comber, These 
structures were already there in the genera and have nothing to do with the axiom 
of competition/selection pressure. Invading the beach just meant for these genera 
invading new terrain, in part unoccupied. The effort often was not even 
considerable, as they remained for their root system largely freshwater plants, 
and for several genera the hot beach conditions did not differ much from their 
main development in dry inland savannahs. 

I could for many other specialized habitats give a similar picture, in the way 
that so-called pre-adaptations were already represented in existing structures 
outside these specialized habitats. A development of large hypocotyls with food- 
reserve in the seed, is for example represented in many tropical inland trees; it 
developed strongly in the littoral Rhizophoraceae, but certainly not as a result of 
competition/selection pressure. In passing: this feature is also not necessary at all, 
as the tiny seed of Sonneratia mangrove trees does not show anything of the kind. 

A similar picture is displayed in almost all ecological specializations, be it 
rheophytes, therophytes, etc. 

It should be added that, whereas the survival level scheme holds for one 
species or group at one time and in one place, the corollary is that patio ludens 
characters may, in later stages, or during migration of a taxon to other places with 


112 Gardens’ Bulletin, Singapore — XX1X (1976) 


different environments be ‘pushed down’ under the survival level as they become 
essential for survival in these stages or places where their latent existence is 
activated. Such characters may be physio-ecological as well as morphological. 

In conclusion: (1) structures originate and may suit more than one ecological 
class or niche, necessarily leading to the peopling of specialized habitats with an 
array of unrelated, ‘generic waifs’ coming up to the minimum requirements of the 
habitat. 


(2) ‘Pre-adaptation’ is often used in a misleading way, as a fancy term 
invented through pre-occupied thought. It should be defined more clearly, as in 
most instances in plants it has nothing to do with adaptation. It should preferably 
be replaced by the neutral term: ‘pre-disposed structure’. 


4. Early differentiation 


The survival level scheme set out in fig. 1 is, of course, meant for one time 
of each plant or animal in one place: it is dynamic, because in the course of time 
the significance of characters will, or at least may change. Structural characters 
as they appear today to belong to a rigid scheme may, in the far past, in primitive 
ancestors not have had the organizational significance they have now. Such 
characters may have been then irrelevant not only in plants but also in animals, 
because the more primitive the organisms are the lower is their survival level and 
the larger their patio ludens must have been. 


I have in this context questioned zoologists in asking why in the great phylum 
of Arthropoda the Insecta are based on an organization scheme with 6 feet, while 
the Arachnoidea are based on a scheme with 8 feet, and whether they assume that 
such a basic structure has been the result of competition and natural selection; their 
answer was in the negative. Similar questions can be asked about the fact that 
Vertebrates all have 4 extremities, Cephalopods have either 8 or 10 arms, that the 
basic scheme of Echinodermata is 5-merous (in an exceptional small group 
‘running wild’ towards an 11-merous structure) and why this would have advantage 
over a 3-, 4-, or 6-merous structural scheme which would equally have been 
feasible. In corals, on the other hand, there are again two large classes, the Octo- 
corallia and Hexacorallia; why are there no Pentacorallia? With the exception 
perhaps of the quadrupedal organization which may be the most ‘economical’ 
solution from the structural point of view as well as for neuro-locomotor organiza- 
tion, these numbers like many others in animals (e.g. 5 fingers in tetrapods, 21 
scleral elements in sauropsids) and like merousness in flowers, appear to be quite 
accidental and devoid of adaptive or selective significance. These structural 
schemes must have been fixed at initial stages, but the agency which caused the 
‘decision’ seems very obscure. Still this decision was extremely important, being 
decisive for later phylogenetic organization. 

It seems a far-fetched idea that this decision had anything to do with com- 
petition/selection; to me it appears a matter of casual structural development for 
which the potential was already embedded in the basic genome matrix, Once 
triggered development could not proceed otherwise. 

In the initial primitive stage these basic structures may well have been patio 
ludens characters of the group concerned, irrelevant of competition/selection 
pressure, similar as must have been the case with many phylogenetic characters of 
plants, as has been advanced earlier in the preceding chapter. 


Autonomous Evolution 113 


This leads then to consider the genetical status of the merousness, and to the 
question: were these characters which have now class or phylum value at the early 
initial stage of much lower genetical value and apt to variation, maybe even at 
species level? How could it then be understood in the genetical sense that, what 
initially was possibly defined by a few genes could later develop into a strictly 
fixed bond characteristic of a whole phylum, and obviously so essentially integrated 
in its genome structure that it was not liable to be influenced by later mutations? 
In fact, except for rudimentation, secondary changes of such accidentally fixed 
primitive numbers are very rare indeed. 


5. Saltatory evolution in plants 


It is axiomatic that structural development is always proceeding stepwise, never 
completely gradual. In this point there can be no difference in inanimate or animate 
chemical compounds: both energy and matter are discontinous, ‘molecular’: 
quanta, atoms, genes, and so their changes must be discontinuous. 


The changes brought about by evolution in organisms can of course be small 
or large; if the steps are very small, the process looks to us gradual and one can 
speak of ‘gliding evolution’; a mutation concerns at least one gene change. But 
if the changes are larger steps, one speaks of saltatory changes and development. 


As in animals evolution in plants starts with divergence, and divergence must 
start from diversity, often called variability, of a genetical nature. 


The first major step to evolution is speciation, that is, changes on the species 
level. This holds for all levels, as the first representative of the suprageneric taxa 
must also belong to a species. The origin of species is thus the most important 
phenomenon in evolution. But what is the criterion for a species, especially its 
delimitation? In two previous essays (1949, 1957) I have extensively treated the 
causes of variability and species delimitation respectively. I have come to the 
conclusion that there are essentially two ways of speciation, viz. through racial 
segregation and through saltation. 


With racial segregation a species population segregates in the course of the 
slow process of dispersion into spatially (ecologically or geographically) isolated 
(replacing = vicarious genetically differentiated ecotypes, races and subspecies, 
in response to the ecological environments in the new lands (see van Steenis, 
1949: xliv—l, and 1957: clxxxili—cxcvi). 


Such raciation may finally result into a compound string or array of ‘beads’ 
representing convivia in Danser’s sense. 


Such races differ from one another in their gene combinations, but these 
differences usually concern only a restricted number of genes and in the intervening 
border zone where two adjoining races meet there is a transition zone where fertile 
hybridization takes place and intermediary specimens occur. On the borders 
marginal differentiation takes place by pioneer advances (genetic drift). 


The general experience in plants is that raciated species populations form 
together one commiscuum (syngameon of Lotsy) in Danser’s sense (1929). Such 
a commiscuum is really a net of interfertility, as all races are miscible with the 
adjoining ones. Even if widely spaced races may become isolated through circum- 
stances, fertility usually remains intact. There are many cases to support this. For 
instance the Pleistocene glacial period has broken up many populations, but through 
this cause now widely disjunct ‘species’ of, for example, Platanus and Campsis, in 
East Asia and America are still miscible; properly they should be treated as races 
of one species population and classified taxonomically as subspecies. 


114 Gardens’ Bulletin, Singapore — XX1X (1976) 


The possibility that the furthest remote races have accumulated so many 
hereditary differences that they prove incompatible if brought artificially into 
contact cannot be excluded. They may still be crossable but not miscible any more, 
that is, in hybridization will not go beyond the sterile F, hybrid. 


I would not go so far as to exclude the possibility that accumulating differences 
in gene composition may, after a long period of isolation, in a restricted number 
of cases lead to new species. This possibility is still more likely if partial popula- 
tions survive in isolation on islands. 


But the general impression is that in plants speciation through racial segrega- 
tion must be a rare phenomenon and that this so-called ‘micro-evolution’, however 
interesting it may be for an understanding of the variability within a species is, 
in plants, of little significance in phylogenetic evolution. Racial segregation is a 
restricting agency, pruning variability; it is in phylogenetical sense not a creative 
agency. Goldschmidt (1933) defined this in saying concisely: ‘‘Geographische 
Variation ist weder eine Vorstufe noch ein Modell des Artbildungsvorganges”’. 


Saltatory evolution appears, on the other hand, to be the common way in 
which form-making in plants takes place, and this can easily be observed from the 
still growing, important body of facts about chromosome numbers. Scanning these 
it is obvious that a very large number of species are polyploids, either autoploids 
or alloploids. Still more interesting is the fact that this increasing information shows 
within families the frequent occurrence of dysploid, aneuploid and allopolyploid 
numbers which are not seldom characteristic of genera of higher taxa. Genera can 
have allopolyploid genomes, as occurs e.g. in Gossypium. 


Cultivated cotton is generally tetraploid (52 chromosomes), and is supposed 
to be an allotetraploid of Gossypium arboreum L. x G. thurberi Tod. (or some 
other Asian and American diploid species) (Brown, 1951). Note that the cultivated 
types are natural allotetraploids and that they behave as diploids. The product 
arboreum x thurberi is not quite similar. 


Stebbins (1971: 179-201) emphasized the important creative role of 
polyploidy in Angiosperm phylogeny and concluded (I.c.: 198) that “extensive 
polyploidy must have taken place during the early evolution of woody Angio- 
sperms. The most probable hypothesis, therefore, is that the polyploidy which gave 
rise to the basic numbers of woody plants took place at various times during the 
Cretaceous and the earliest part of the Tertiary Period, while the diversification 
of species on the basis of secondary basic numbers is largely a product of the 
Tertiary and Quaternary periods’. He cited many examples of tropical taxa in 
this context and estimated that between one-fourth to one-third of the flowering 
plants are polyploid with reference to their nearest relatives. 


In some families taxonomic affinities can thus be supported cytogeographically 
and attempts can be made towards a reasonable reconstruction. See for instance 
the most interesting papers on Australian Proteaceae by Johnson & Briggs (1963), 
on Pomoideae by Challice (1974), on the Casuarinaceae by Barlow (1959), the 
Loranthaceae by Barlow & Wiens (1971), the Oleaceae by Briggs (1970), and the 
Malvaceae by Bates (1968). ‘ 


There are at least two processes by which chromosome changes are brought ; 
about, viz. hybridization (proved in many cases) and obviously irregularities in 
meiosis (translocation or ‘centric fusion and fission’, aneuploidy, duplication); 
there may be others. 


The main point is, that major genomic rearrangements of the type quoted 
above, occur in a single generation, indubitable proof that saltatory form-making 
has been the major feature in plant evolution. See fig. 2. 


Autonomous Evolution 115 


comm.6 


0 
E 
E 
(eo) 
oO 
| 
| 
| 


comm.1 


— 
— eee 


Fig. 2. Scheme of saltatory evolution in plants by individuals. 


Commiscuum I has produced the daughter commiscua 2, 7, and 8. Commiscuum 2 has 
produced the daughter commiscua 3, 4, and 5. 


Commiscua 1, 7, and 8 show mutual affinity and so do commiscua 2, 3, 4. 


Commiscuum 6 is an allopolyploid between commiscua 3 and 5; it shows affinity with 
several other commiscua but is also an example of reticulate phylogeny. 


Even though they may not become established at once, they certainly re-occur 
with a given probability and sooner or later will result in a population of indivi- 
duals with novel characteristics. Thus, the idea seems justified that evolution in 
plants is largely of a saltatory type. For instance, polyploidy undoubtedly has been 
instrumental in many cases, in producing new forms. Some botanists claim that 
autopolyploids are side-products of evolution, being variations on a given level 
only, whereas evolutionary progress occurs on the diploid level. There is on the 
other hand no doubt that amphidiploid combinations are significant in evolution. 
More importantly, saltatory genomic changes in the diploid range are well- 
documented, especially in the genus Clarkia (Lewis, 1953). 


In any case it appears that such evolutionary changes have nothing to do with 
competition pressure or selection of the fittests. 


Naturally, the fit survives, the new plant arisen must come up to survival level 


and be able to germinate, grow, and propagate, but that is all there is to it, harmless 
extras are allowed. 


116 Gardens’ Bulletin, Singapore —- X XIX (1976) 


It is admitted that not all families show an important array of ploidy variation, 
e.g. Pinaceae or Lauraceae seem to be exceptions. In the Lauraceae the family 
number seems to be x = 12, including the vegetatively aberrant parasitic, herba- 
ceous genus Cassytha, according to Okada & Tanaka (1975). Incidentally, this 
number seems to be common in primitive Angiosperms. In such cases the number 
of chromosomes does not tell much, and information would be needed about the 
internal structure (chemical composition) of the chromosomes and also about the 
way in which these ‘internal’ differences have come about. The same should be said 
about genera in which the number of chromosomes is very constant; sometimes 
differences in size and shape already reveal this in a superficial way. The study of 
the genome architecture in plants is of course a most difficult field to explore and 
we are only beginning to enter it, for instance by measuring DNA hybridization. 


Finally I would here also remark on the phenomena of teratological and 
neotenous forms, for which I refer to my essay of 1969. Teratological forms arise 
as sports all of a sudden. With teratological forms it is clear that physiological 
chain-reactions in plants have undergone change. Classes of terata so much resemble 
taxonomical characters (prolification, antholysis, enations, cohesions, fasciation, 
laciniation, adesmy, reduction, petaloidy, scyphogeny, and ceratomania) that they 
cannot simply be ignored or waved away. Some terata are known to be inherited 
and due to a single gene mutation. Bringing terata and: phylogeny in line means 
that they should be hereditary (see e.g. Stubbe, 1966). 


The concept of terata is mostly accepted as something ‘abnormal’ or 
‘monstrous’, and should be disposed of as meaning inferior. This appears to me a 
very superficial, emotional evaluation. Many evolutionary processes are brought 
about by reduction, suppression, fusion, etc.: a panicle of separate flowers changes 
into a head or fig, or is reduced to a raceme, or even a single flower; meristems are 
suppressed and contraction follows; or they are joined to other meristems and 
fusion follows (ovaries of Morinda; epiphyllous flowering; concaulescence in 
Solanum, etc.); leaf production is suppressed on twigs which grow into thorns: 
lateral branches do not develop inflorescences and are metamorphosed into curved 
hooks for climbing (Uncaria). There is no end to these metamorphoses, each of 
which represents an ‘abnormality’ or ‘malformation’ if compared with that of the 
immediate ancestor which did not possess the new structure. Thus the ‘concept’ 
of terata has a very definite structural meaning in biology, viz. a sudden change 
of structure which differs from the taxon from which it evolved. 


Comparing trees of the Naucleeae with the miserable Uncaria, a climbing plant, 
of which part of the flower-bearing side-branches are flowerless and deformed into 
curved hooks, the latter is an abnormality; but surely Uncaria has found its niche, 
proved its vitality and developed into quite a large genus. Considered unemotio- 
ese from a broad outlook, systematical teratologies are really hereditary terato- 
ogies. 


Many of these changes are morphological reductions or suppressions, and 
that stamps them to belong to neotenous behaviour, that is: reaching maturity 
before all parts have developed as in the immediate ancestral form, Precocious 
flowering may turn a woody plant into a herb; precociously flowering herbs may 
be reduced to flower production on the cotyledons of the seedling (Monophyllaea). 


For plant evolution I ascribe (1949, 1969) great importance to neoteny 
which I regard as one of the two crucial processes in their evolution. Takhtajan 
(1954) spoke of ‘phylogenetic teratology’ and correctly generalized and applied 
it to all contractions and reductions, as a vital element in form-making. 


Systematical teratologies originated in all probability suddenly as saltations, 
in one or more steps and survived if they were viable in the sense that their 
ecological and reproductive capacity reached survival value, with their morpho- 
logical caprices tolerated. 


Autonomous Evolution 117 


In contrast with the chromosome ‘mutations’ caused by hybridization or other 
mutative changes I have the conviction that important changes in morphogenesis 
might often have been caused by not too integral genetical changes. I derive this 
from the fact that fasciation (as in Celosia cristata L.) or pelorial flowers (as 
occur in Scrophulariaceae, Orchidaceae, etc.), which give a fundamental change 
to structure, seem to be based on presence or absence of one or very few vital 
genes only. 


I once discussed with a famous botanist how he thought that a pitcher of 
Nepenthes might have originated. To my surprise he said that this might have been 
gradually built up, may be by a thousand gene mutations. Obviously he was 
ignorant of scyphogenous structures in the cultivated ‘crotons’, fancy varieties of 
Codiaeum variegatum (L.) Bl., in which the rough skeleton of a Nepenthes pitcher 
can be observed, the blade, tendril (naked midrib) and at the end a pitcher with an 
appendage (the lid). 

If such a structure can be formed in a ‘sport’ of one known species, little 
imagination is necessary to assume the origin of a pitcher, through scyphogenous 
action, in a few saltatory steps. Once the initial step was made, autonomous 
perfection can be imagined in a few more orthogenetic steps. 


Blocking of certain vital genes by mutation may cause development to follow 
another physiological pathway in the chain-processes leading to morphogenesis 
and production or reduction of proteins, hormones or other substances controlling 
form-development. 


I have talked about this matter with geneticists, both on the matter of stability 
of structure and obviously responsible genome patterns on one hand, and sudden 
changes in a few vital genes on the other hand, but it seems that these seemingly 
contradictory phenomena cannot easily be translated in genetical terms of 
molecular biology. They find this a most complicated matter about which even 
generalized ideas of morphogenesis in genetical terms can not yet be given. 


However unfortunate this may be, I hope the meaning of the arguments given 
above is clear. They lead to the following conclusions: 


(i) In both major causes of evolution of plants, that is either changes in the 
gross chromosomal patterns (allopolyploidy, dysploidy, aneuploidy) or the 
physiological function changes of morphogenesis by neoteny, the changes are 
sudden, saltatory. 


(ii) The saltatory steps are at least at species level, but higher categories, for 
instance genus level, may also be involved. 


(iii) The conclusions given above imply that evolution of plant structure is 
essentially not caused by competition but is an autonomous process in which 
chance plays a distinct rdle. 


(iv) For form-making the gradual accumulation of gene changes resulting 
into raciation may not be excluded as a cause of segregation of species but should 
be considered as of minor importance, while also their competition is not the 
overwhelming agency as frequently supposed. 


In fig. 2 I have drawn a scheme reflecting the above considerations. 


6. Gliding evolution in animals 


As explained in the introduction the mechanism of evolution in animals must 
be much more complicated than in plants, as in addition to autonomous develop- 
ment in patio ludens at early stages it must include competition. As in most plants 
raciation in species populations easily occurs, sympatric and allopatric, the main 
difference with plants being that such raciation is largely a matter of competition 
partially for food and shelter, but with the additional agency of sexual selection, 


118 Gardens’ Bulletin, Singapore — X XIX (1976) 


which is absent in plants. Through these combined factors and competition racial 
segregation will in animals usually develop more rapidly than in plants. By this 
sexual selection partial populations drift apart and become in the practical sense 
incompatible, and thus a start is given to divergent development. In several cases 
it has been shown experimentally by artificial insemination that recognized good 
species of insects, which in nature keep strictly apart, are factually compatible. 
But through their isolation by sexual selection and then occupation of a specialized 
ecological niche they will finally drift apart, by populations, to such degree that they 
become incompatible genetically. Thus they start as convivia but gradually become 
commiscua and finally comparia, to stand on their own for future development. 
Mutations irrelevant to survival will be possible, but these will play a much smaller 
role than in plants as patio ludens in animals allows for much less free form 
development than in plants by predominant competition and sexual selection 
pressure: any new feature arising is ‘tested’ on its usefulness for competition. 
See fig. 3. The reader may recall that a prominent zoologist and geneticist, 
R. Goldschmidt, has put forward the idea that in the macro-evolution of animals, 
saltatory re-arrangements of the genome, and ‘teratological’ mutations “‘the hopeful 
monster’) have been important. But there seems to be little evidence to support 
this concept. 


Fig. 3. Scheme of two initial stages of divergence in the gliding evolution of animals by 
populations. 

A. A mother population (m.p.) starts to form a convivium (c.v.); it is still loosely con- 
nected and compatible with the mother population by a transition zone (f.z.) of rare misci- 
bility. 

B. In a further stage the convivium of fig. A has developed into a new independent 
commiscuum (comm.) which has become incompatible (indicated by a ‘gap’) with the mother 
population (m.p.). This new commiscuum is undergoing in its turn a similar differentiation 
and has formed a new convivium (c.v.’) comparable to the scheme in fig. A. 


The main conclusions on the differences of animal evolution as compared with 
plants appear to be fourfold: 


(i) Evolution in animals will be gradual, through accumulation of competition / 
selection characters by ‘gliding evolution’, through separation of divergent popula- 
tions, raciation with practical incomptability into convivia which gradually develop 
into truly incompatible commiscua, and finally into comparia. 

(ii) Evolution of animals goes in general by populations and not by individual 
specimens as usual in plants. 

(iii) There is little opportunity for patio ludens characters to develop, as all 
are tested on usefulness for competition and survival, and are subject to sexual 
selection which is unknown in plants. 


Autonomous Evolution 119 


(iv) Saltatory steps are not excluded, but they must be extremely rare in 
proportion to their frequent occurrence in plants, 


In fig. 3 a scheme has been drawn reflecting these considerations. 


7. Co-evolution of animals and plants 


As I have emphasized in the first chapter plants were the first organisms of 
all organic evolution by their capacity of assimilation, capturing and storing 
energy. Animal life developed later, and never became independent. Food chains 
always have to go back on plant life. 


Animals could in a broad sense be considered to lead a parasitic life; they 
browse and feed on plants which make their life possible. 


Except for negligible exceptions plants play the passive rdle, and the organic 
matter they produce is at the disposal of animals which are specialized for taking 
advantage of anything they can find, even the most indigestible organic products. 
From this follows that plant evolution goes independent of animal evolution and 
that novelties arising in plants are secondarily exploited by animals. Notable 
exception: a large part of Angiosperm evolution has been aligned to pollination 
‘symbiosis’ with animals. 

Apart from the plant bodies themselves, used as food, animals are attracted 
to them by colours, scents, and obvious shelter. Evolutionists seem generally to 
assume that glands, floral and extra-floral, give competitive advantage to plants 
through the prowling animals. They have theorized that in such a way the 
competition/selection principle was forced on the plants, inducing plants to excrete 
more nectar or other substances, and thus induce numerical advantage over those 
which produced less, or less abundant, attraction to animals. 


This is a very crucial problem indeed, and it seems difficult to prove or to 
disprove whether the assumption of this advantage is true or not, and that it 
worked under natural conditions. 


For one thing, experiments lack of course the factor time. Even if it were 
proved that there was advantage to plants by animals this would mean that this 
assumed advantage would result into greater numbers of the plants (higher popula- 
tion density) which had the advantage. It is hard to believe, however, that this 
would mean extinction of those which offered less benefit. The latter would have 
a lower population density, but we can observe that precisely such a phenomenon 
is ubiquitous in the plant kingdom. In each genus certain species are rarer than 
others, but it would be a far-fetched idea that all the rare or rarer ones are nearer 
to, or nearing extinction. This is largely a matter of ecology, available niches, etc., 
not an immediate result of competition pressure: each species has its own ecology, 
including frequency of occurrence. 


For another thing experiments never reflect the situation in nature. Imagine 
an experiment in which seeds of two allied species were sown together with the 
result that the seedlings of the one crowded out the other. Would it be conclusive 
to speak of higher competitive value and selection? It would certainly not be 
conclusive, except for the experimental conditions, the soil used, etc., and not for 
the varied conditions nature offers to the two, where such situations as in the 
experiment will hardly ever occur, and then only extremely locally, if ever. The 
very existence of the two species disproves already the assumption: in nature both 
occupy obviously their own particular ecology, otherwise one of the two would 
not exist. 


Excretion in plants is mostly a physiological necessity. Dripping from 
hydathodes occurs when evaporation is insufficient: organic and mineral substances 
excreted in this way may serve animals. A similar reasoning could be held for 
excretions by glands. 


120 Gardens’ Bulletin, Singapore — X X1X (1976) 


Shelter is ‘offered’ by plants to animals, in many ways. 


On the under-surface of leaves a fairly large number of woody plants develop 
domatia in the axils of the main nerves. The physiological] function of these domatia 
is not known, according to Jacobs (1966), who published a classic paper on 
them. They do not excrete and are not glands; they appear often only when seedl- 
ings have reached a certain age. Their distribution in the plant kingdom is large 
but restricted; they have never been found in plants of arid countries. They were 
not infrequently termed ‘acarodomatia’, derived from the observation that small 
arthropods seek shelter in these small cavities. It is proved that they originate 
irrespective of animal irritation and appear to be a whim of plant structure. The 
fact that animals exploit them as shelter means nothing special: animals will of 
course exploit anything they find favourable for their comfort and survival, 
animate or inanimate, just as primitive man would employ anything which he 
found useful or of advantage. Our urgent strife of locating useful things is of course 
not different from the same urge in animals. In fact we and the animals are 
completely possessed by this strife. But from a strictly detached point of view 
there is every reason to accept that domatia are an irrelevant structure in plants 
which is secondarily exploited by animals. That is, if we really want to detach 
ourselves from the inherent prejudice that all characters of animate nature must 
have some useful meaning. 


I am of course by no means the first who ventilates criticism and in this 
context I want to refer to Bateson (1894: 12) who “undertook the study of 
adaptation as a test to the theory of natural selection and the hypothesis that there 
is a tendency for useful structures to be retained and for useless parts to be lost. 
We have no right to consider the utility of a structure demonstrated, in the sense 
that we may use this demonstration as evidence of the causes which have led to 
its existence. In absence of correct and final estimates of utility, we must never use 
the utility as a point of departure in considering the manner of its origin. It thus 
happens that we can only get an indefinite knowledge of adaptation, which is not 
an advance beyond the original knowledge that organisms are more or less adapted 
to their circumstances. No amount of evidence of the same kind will carry us 
beyond this point’’, 

If we cannot perform this mental effort towards objectivity we will have to 
account for the presence of hairs, stipules, phyllotaxis, etc. etc. as well as for their 
absence in terms of utility. ““No doubt’, Bateson (1894: 79) says, “that ingenious 
persons would find ecological explanations of all these characters, for on this 
class of speculation the only limitations are those of the ingenuity of the author’’. 


Various kinds of shelter are employed by ants in tropical plants, In these 
myrmecophilous plants the devices may be very simple, stem-appressed leaves of 
root-climbing plants (Hoya, Dischidia), reflexed appressed lowest pinnae of palm 
fronds (Calamus sp.), palm-sheaths (Korthalsia), appressed stipules, saccate 
domatia (several neotropical Melastomataceae, Callicarpa saccata van Steenis), 
but also pithy stems (Cecropia, Endospermum spp., Clerodendrum fistulosum 
Becc.) and pithy branches in a large number of Malesian trees of various families, 
the tendril of one species of Nepenthes, and stipular thorns of Acacia, in which the 
pith is removed to shelter ant colonies, The most spectacular shelter is offered by 
the root tubers of the epiphytic rubiaceous genera Myrmecodia, Hydnophytum and 
some allied genera. These tubers have large labyrinth-like cavities inhabited by 
ant colonies where they tend fungal gardens as food. 


There is a host of literature on this subject, a survey of which would fill a 
book in itself. The essential question turns round the adaptation theory of Beccari 
(1884-1886) and Schimper (1888) who advanced that such structures in plants 
arose by the mutual action of plants and animals to the advantage of both. And 
they tried to collect data to show the advantage of ants for plants. The latter 
evidence appears, however, very dubious indeed. 


Autonomous Evolution 121 


One crucial point has been cleared by Treub (1883) who showed that the 
cavities in the Myrmecodia tubers originate already in seedlings without any action 
of ants and excellent upgrowth follows without them. Whether these cavities have 
any ecological meaning to the plant is uncertain; they may physiologically serve 
for aeration or evaporation for regulation of temperature, but this has not been 
proved. 


It is doubtful even, whether they are essential to the ants. We note in this 
context, that certain European ants build their nests around the base of plants. 
preferably Rosaceae and Umbelliferae, but they survive equally well without them. 


It stands to reason, however, that in an objective view there is no necessity to 
assume co-evolution, if we advance that these structures would also have been 
developed by plants without any ants in existence. Why should not leaves be 
appressed to stems in root-climbers, stipules leave cavities, leaves have domatia, 
pinnae be reflexed, stems and thorns have pith, all representing structural develop- 
ments sui generis? 


Conversely, it is clear that if ants evolved and would find these structures, 
they would employ them and take full advantage. Some species might even become 
entirely dependent. 


Plant structure evolves first and it is the animals which will adapt themselves 
and often will evolve to greater specialization. This principle applies to chemical 
differentiation as well. 


It has sometimes been advanced that the supposed profit the plants would have 
from the ants would consist of protection against other predators, but this is 
proved to be a fallacy. For Myrmecodia the profit for the plant was supposed to 
consist in accumulating minerals etc. for growth, but there are many large woody 
epiphytes without ants showing that in this aspect epiphytes can well manage this 
themselves. Then it was advanced that for several other myrmecophytes the ants 
are attracted by their seeds with their oil-containing elaiosome, which seeds are 
deposited in their nests. This is true and may locally add to their frequency, but 
none of these ant plants is confined to ant nests and their seeds can germinate on 
any suitable bark. 


It must be concluded that the co-evolution of ants and plants is only a one- 
sided evolution, namely for the ants. 


I fully agree with von Ihering (1907: 710) who said that Cecropia needs its 
ants as much as a dog its fleas. 


Evolution of orchids 


The spectacular development of Orchidaceae is of course a classic of 
co-evolution. Leaving apart a fairly considerable number of orchids which are 
self-fertilizers or are cleistogamous, the majority is compulsory cross-fertilized by 
insects and this has led to most ingenious devices of the orchid labellum. 


Systematically the queer fact is that in orchids so many generic hybrids are 
found, and that still more can be made by artificial insemination. The definite 
impression is that the whole of the family is genetically only one comparium with 
many commiscua, and that the species are usually convivia, They maintain their 
distinction by the grace of compulsory cross-pollination and the use of selected 
Insect species to achieve that goal. Orchid evolution thus reflects insect evolution. 


_ As soon as in the variability range of an orchid a deviation, differing only 
in a few genes presumably, occurs, it may be favoured with an insect form from 
the variability range of the latter’s population and the two will consequently form 
a couple of consorts. This is the first step towards more specialized couples of 
orchid /insect. 


122 Gardens’ Bulletin, Singapore — X XIX (1976) 


Here again, however, the deviating plant structure comes first; if there is no 
suitable insect partner, it will probably succumb; if there is a more or less suitable 
partner attracted by colour, shape, scent, etc., within the range of variability of the 
insect population, the couple is formed and the new plant is saved and lives on by 
the grace of the pollinating insect. The latter is of course in no way dependent on 
the orchid for its survival. 


It cannot be the reverse, as there can be no stimulant or inductive influence 
emanating from an insect causing a plant towards a gene combination which it 
wants to have. Plant structure comes first, animal adaptation may follow. 


Though we conclude that thus evolution in orchids will have been effected in 
a gliding way, imitating that of animals, saltations may occur by hybridization, It 
is namely known that insects may, incidentally, make errors in pollination by 
which even intergeneric fertile hybrids may occur. Their offspring will in subsequent 
generations produce a host of new forms which may again start couples with other 
insects and consequently lead to further form-development. 


This sudden occurrence of hybrids may be termed ‘saltatory’, but for the 
essential difference that the saltation is of a much lower status than that discussed 
for other plants, as all the offspring remains within the orchid comparium in a net 
of interfertility. 


A further curious observation can be made in orchids, viz. that by a single 
other ‘saltation’ the orchid flower does not develop in the proverbial bisymmetrical 
way, but as a normal regular monocotyledonous flower. Such ‘peloric’ forms, of 
which I have formerly listed some from the tropics (1949: xli-xlii), are only 
recognizable vegetatively by comparison, otherwise they are unidentifiable, even 
by first-grade specialists. 

Whereas pelorias are generally caused only by one or a very few gene 
changes, this tallies with the considerations above that obviously the most 
remarkable build-up of the orchid labellum may be a beautiful facade, but that 
it is genetically and hence, taxonomically, not such a stable component. 


It shows also that few genes may, in cases, bring about a sudden radical 
change in morphogenesis, 


Evolution of figs 


The evolution of figs is a culmination point of co-evolution, as here the 
pollinating wasps have still more specialized relations with the plant in that also 
their life is bound to the figs in a most intimate way, a compulsory symbiosis. This 
is certainly not so with orchid insects, not even in the highly specialized cases of 
pseudo-copulation, Much of what I have said about the relations between orchids 
and insects will hold here too. 


New forms of Ficus will arise and succeed if from the variability of the insect 
populations a more or less suitable mate is available. If it is available, adaptation 
of a new insect population will follow. Much of this evolution seems not to have 
been competitive. Evolution seems to have resulted from the “‘extremely gradual 
alteration of the Ficus-protoplasm’”’ (Corner, 1961: 113). In this aspect it is 
noteworthy that all species of Ficus seem to have the same chromosome 
number, x = 13. ) 

If this assumption is true it would theoretically follow that artificial insemina- 
tion of closely allied species of figs would in all probability lead to fertile hybrids. — 
I am not aware that such crucial, certainly difficult experiments have ever been © 
carried out. hs 

A conclusion on this chapter on co-evolution runs as follows: 

(i) In a large number of situations attributed to co-evolution, evolution is — 
primarily of the animals. Plant structures are utilized by animals for their benefit 


Autonomous Evolution 123 


and they specialize. The plant structures arose sui generis and not in so-called 
‘response’ to animal agency. 

(ii) Even in the vital association of insects and flowers in orchids and insects 
and figs in Ficus plants change (evolve) independently in an autonomous way 
and insects adapt themselves. 


(iii) Speciation in orchids and figs imitates (follows) the gliding evolution 
as is usual in animals. Small changes accumulate in populations which diverge and 
gradually develop into races, subspecies and species respectively which in nature 
gain (ecological) isolation through the coupling with the particular insects. Insects 
are thus secondarily stimulated towards further evolution themselves. 


(iv) Saltatory evolution in both groups, more especially in orchids, may occur 
incidentally through hybridization. 


8. Reticulate phylogeny 


I have termed this chapter reticulate phylogeny instead of reticulate affinity, 
because it concerns real ancestry which is meant here. 


In general plant evolution through speciation will run divergent as in the 
branching mode of a tree, similarly as in animal evolution. Fig. 2. 


There are, however, many instances known of allopolyploid species hybrids 
which are truly new species; they certainly in part share the characters of the two 
parent species but exhibit also new characters of their own. 


By definition genetical contacts are prohibited between comparia. In plants 
a comparium is not rarely equivalent with a subgenus or genus, and as a rule 
species of different genera are incompatible and merging or exchange of genetical 
material is excluded. 


However, exceptions occur, and there are several cases known where clearly 
through previous hybridization different generic genomes were blended through 
allopolyploidy. In the Cruciferae an allopolyploid generic hybrid was made between 
Brassica and Raphanus. Many genera are supposed to have originated in this way, 
e.g. Armoracia, and certain allopolyploid species known in Gramineae from 
parents belonging to different genera, such as Aegilops and Triticum, Agropyron 
and Elymus, etc. As early as 1881 Focke mentioned generic hybrids from the 
families Amaryllidaceae, Cactaceae, Campanulaceae, Compositae, Ericaceae, 
Gesneriaceae, Rubiaceae, and Scrophulariaceae; others have been found since. 
This opens the possibility for allopolyploidy. 


_ I would certainly not suggest that all cases of reticulate affinity, a phenomenon 
which occurs frequently in plants, should be deemed to be the result of reticulate 
phylogeny. 


On the other hand I suppose that in very many cases allopolyploid genera and 


species have as yet not been recognized as such and my estimate is that there is 
a fair number of them. 


Allopolyploid blending means that two divergent ‘twigs’ of the ancestral trees 
are joined which caused a local ‘netting’ of its ‘canopy’. There is good reason to 
suppose that this ‘intertwining’ has also acted in the past during the ancestral 
development of the plant kingdom. See fig. 2. 


I emphasize that these allopolyploids may be extremely important in plant 
evolution, as from them other types, aneuploid, dysploid, or polyploid, may have 
originated. 

_Compared with plants such reticulate phylogeny may be tacitly assumed to 
be in the great minority in animal evolution. This is quite obvious, because sexual 
selection will prohibit to no mean degree genetical contacts at the level of species 


124 Gardens’ Bulletin, Singapore — X XIX (1976) 


and genus. It makes it especially unlikely, or very rare, because in animals sexual 
behaviour, attraction and structure of the sexual organs play such an important 
role in the divergence of populations. Many ‘experimental’ specific and few generic 
hybrids are known, especially among insects, birds and mammals. But they are 
sterile as a rule, and even hybrids on a racial or sub-species level in the animal 
kingdom are very often sterile, a situation which is exceptional among plants. 


9. Embryology and ontogeny 


The fact that embryological and subsequent ontogenetic development in 
animals is so different from that in plants must have had evolutionary implications. 


In animals the development of the embrvo leads via metamorphoses, even- 
tually alternated by larval generations, to the mature stage, but from the start it 
concerns the whole individual and its complete organization. This changes and 
grows and differentiates by a long series of internal structural transformations; 
it is a closed system. It is thus quite conceivable that for animals the subsequent 
stages in ontogeny can to a certain degree reflect the sequence of phylogenetic 
stages, as defined in Haeckel’s principle or law of biogenetics. It can also be 
assumed that genetical changes may occur at all stages of this ‘centripetal’ 
development. 


This is essentially different in plants where development is centrifugal and 
structure is proportionally so simple. Though the individual in statu nascendi is 
as the embryo contained in the seed coat, the internal development concerns only 
the development of the archegonium to a mature seed, There is no question of 
further internal transformation; it is an open system, Reserve food is stored either 
in albumen or cotyledons or both, but there is no reason to assume that either of 
the two is a reflection of ancestry in shape or otherwise. It should be admitted that 
a few ancestral characters e.g. primary vascularization, may be preserved as vestiges, 
as in plants all parts are end-products preserved thanks to the presence of cell- 
walls. 


Also the first leaves above the cotyledons cannot be seen as reflecting 
ancestral shape. The ancestral, primitive shape of the leaf in Angiosperms is, as 
Corner (1954) has argued, in all probability the compound leaf, as still retained in 
many tree families as a primitive character, token of possible derivation from 
compound-leaved seed ferns. It is not impossible that also the seed ferns had 
seedlings with simple leaves and that the whole complex of vegetative upgrowth 
of seed fern ancestors is grosso modo retained in certain woody families of 
Angiosperms, 

Under this point of view the simple leaf is among Angiosperms a derived 
stage. Such reduction should be considered as a manifestation of neoteny 
(see p. 116) by which principle is meant that the new form is simplified as 
compared with its ancestor at attaining the fertile stage. Neoteny causes ontogeny 
to be condensed; it is probably as frequent in plants as it is in animals. 


The matter considered in this essay has lingered in my thoughts for many 
decades, in fact since I was a student and studied Carl von Naegeli’s ‘Mechanisch- 
physiologische Theorie der Abstammungslehre’. I realize very well that it will be 
provocative to those thinking in neo-Darwinistic terms. 


For these reason I felt it not unnecessary to feed some ideas to the biological 
world in honour of Professor Corner as a token of my admiration for his immense 
achievement in botany from his studies in the tropics and his admirable attempts 
to pour new wine in old vessels of biological theory. 


I feel much indebted to my friend and colleague, Prof. Dr. H. Gloor, Geneva, 


for improvement of the text. 


a 


Autonomous Evolution 125 
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On Speciation in the Humid Tropics: some new data 


by 
ANDREY A. FEDOROV 


Komarov Botanical Institute, Leningrad 


During the author’s travels to Sri Lanka (Ceylon) and to Indonesia and, 
particularly, in the course of his examination of herbaria and botanical iconography 
pertaining to Dipterocarpaceae (see Foxworthy, 1927, 1932; Van Slooten, 1932, 
1940, 1941, 1942, 1952; Symington, 1943; Ashton, 1962, 1964, 1967, 1969) he has 
already established many facts elucidating speciation in the humid tropics on the 
basis of the Law of Homologous Series in Hereditary Variation discovered as early 
as the beginning of this century by N. I. Vavilov (1920, 1922), elaborated by him 
somewhat later (1930, 1935) and subsequently by his numerous collaborators and 
pupils. 

As is well known, Vavilov established this law mainly in the course of his 
studies on cultivated plants, his attention being attracted by their infraspecific 
diversity. But Vavilov had no opportunity to observe this phenomenon in a 
sufficiently large number of species of wild plants, nor those belonging to perfectly 
homologous genera. 


Vavilov was sure that no homologous series of hereditary variation had been 
discovered in our wild holarctic genera and species merely because, in this respect, 
they had been extremely poorly studied. 


In the Holarctic it is difficult to find homologous variation not only at the 
specific level, but at the infraspecific level as well. Many wild species occurring 
there appear to be surprisingly homogeneous. The cause of the apparent homo- 
geneity is associated with their heterozygosity as has been pointed out by Vavilov 
himself (Vavilov, 1936, pp. 78-79) with cross-pollination, with the latent state of 
their recessive characters. However, the latent diversity of characters can be made 
apparent by means of compulsory self-pollination, or inbreeding. This fact is well 
known by all the geneticists and plant breeders. 


Besides the actual homogeneity there is a delusive homogeneity. A conviction 
is very widespread among taxonomists about the perfect homogeneity of many 
widespread species over vast areas. The reason is that many botanists work mainly 
with herbarium material. The uniformity of herbarium specimens, sometimes 
accumulated in large numbers can be explained by the fact that many collectors 
involuntarily discarded specimens inconvenient on account of their dimensions or 
some other characteristics and thus made collections of standard specimens suitable 
for drying and mounting on standard sheets of herbarium paper. 


As I know, tropical herbaria differ in this respect from holarctic ones. It is 
difficult to sort out series of standard samples in the tropics, even though the 
desire to do it be very keen, since many species, particularly large trees are so 
Sparsely scattered in a tropical forest, that sometimes herbaria contain only their 
type or isotype specimens, This precludes the possibility of revealing infraspecific 
Systems of hereditary forms in these plants by means of sheer observation even if 
they actually exist in nature. 


There are at least a few genera of plants indigenous to the northern part of 
the Holarctic in which homologous series are observed not within species but 


127 


128 Gardens’ Bulletin, Singapore — X XIX (1976) 


among the species of the given genus. Such are the genera Verbascum and Celsia 
(Scrophulariaceae) and Astragalus and Oxytropis (Leguminosae). It is true that 
here the taxonomic delimitation of these genera is not perfectly reliable, however. 


The state of affairs in the humid tropics is very interesting. I venture to assert 
that, within the family Dipterocarpaceae. almost all the representatives of which 
are confined to tropical rain forests of Southern and South-Eastern Asia, the law 
of homologous series is conspicuous in all the genera and numerous species belong- 
ing to this family, including the monotypic genus Upuna, the single species of 
which, U. borneensis, also exhibits homology, at least in the leaf structure, as do 
the species of the other genera of this family. 


It should be pointed out that Vavilov anticipated all this on the basis of his 
theoretical considerations with respect to plant taxa of almost any rank, having 
emphasized the universal significance of the law he had formulated, but practically 
he had no opportunity himself to encounter such interesting material for investiga- 
tion as the Dipterocarpaceae. 


The genetic affinity of the genera of Dipterocarpaceae is so close, that almost 
all the characters pertaining to the shape and structure of leaves, fruits and other 
organs and parts are subjected to homologous variation except the main generic 
characters felicitously designated by Vavilov as “generic radicals”. 


It is only the existence of such radicals, sometimes not quite distinct and also 
transgressive (e.g. genera Shorea, Hopea, Doona) that made it possible to classify 
the Dipterocarpaceae family, comprising a total of up to 580 species, into 15 
genera. 


Owing to the indistinctness of certain generic radicals (or, more precisely, 
unsuccessfully distinguished genera) taxonomists classifying Dipterocarpaceae were 
compelled to reduce to synonyms certain taxa described earlier at the rank of 
genus. Thus disappeared such generic names as Pachynocarpus, Richetia and some 
others. 


When I am writing about the family Dipterocarpaceae, I have in mind only its 
Asiatic subfamily Dipterocarpoideae comprising the greatest number of genera and 
species, leaving aside for the time being the African subfamily Monotoideae (48 
species of the genus Monotes and 4 species of the genus Marquesia), since I have 
not the necessary material at my disposal. The law of homologous series is manifest 
within the Dipterocarpaceae with the utmost distinctness and cogency in the first 
place in consequence of the numbers of species in many of its genera (see Ashton, 
1964; Willis, 1966). 


Shorea ie ba ... 180 Doona bm sain 

Hopea (including Balanocarpus) .... 90 Parashorea ... «sb fou 

Dipterocarpus rit ... 76  Dryobalanops sf 9 

Vatica a4! re ... 76 Cotylelobium 5 

Vateria (incl. Stemonoporus) + sneha tls nf CM acme wide a 3 

Anisoptera on ... 13  Monoporandra 2 
Upuna ... ne De 


If all these genera of Dipterocarpaceae were arranged in a table following the 
sample of similar tables presented in Vavilov’s works, it would at once become 
obvious that with respect to all the characters (studied up to the present time) 
species within each genus form homologous series. 


The table does not show the combinations of characters of particular species, 
but only lists individual characters and their occurrence in the genera. Further- 
more, they are only the most conspicuous ones, revealed either from herbarium 
material or from drawings published in the botanical literature. Many characters, 


Speciation in the tropics 129 


such as the leaf pubescence, the details of venation etc., are still to be studied. It 
is important to point out, that the characters of many species presented in the 
table were observed in isotype specimens a fairly great abundance of which is 
available in the Herbarium (LE) of the Komarov Botanical Institute of the 
Academy of Sciences of the USSR in Leningrad. The numbers of isotype specimens 
found there are 30, 15, 22, 13, 12, 5, 8, 3, 2, 3 and 2 for the genera Shorea, 
Hopea, Dipterocarpus, Vatica, Vateria (= Stemonoporus), Anisoptera, Doona, 
Parashorea, Dryobalanops, Cotylelobium and Monoporandra respectively. This is 
some guarantee against errors in the identification of numerous other specimens 
deposited in the Herbarium as ‘ordinary’ specimens and examined in the course of 
my investigations. 


The table, the principle of composition of which is described here does not, 
of course, deal with the infraspecific homologous variation as yet unstudied at all 
in the representatives of the Dipterocarpaceae. My purpose was to demonstrate 
homologous series of species within genera, which in their turn are also homologous 
to the same extent. Thus, I do not merely repeat what has been done by Vavilov, 
but, as far as possible, endeavour to develop his theory. 


Homologous characters are given in Latin terminology. The best illustrations 
of these characters might have been the drawings or photos, but, unfortunately 
they would have been too numerous and there would not be enough place for all 
of them in the table. 


Unfortunately the names of the examined species not indicated are omitted 
but I hope I shall be able to add them in the very near future in a separate paper. 


Similar to infraspecific systems of the forms of cultivated plants studied by 
N. I. Vavilov, the homologous characters in species belonging to the genera of 
Dipterocarpaceae exhibit in many cases independence of other characters, but in 
approximately 50% of species a rather distinct correlation is observed; for instance, 
between the characters of leaves on the one hand and, on the other the characters 
of fruits, with respect to their general similarity of appearance in the first place, 
and to their equal relative and absolute dimensions as well. 


Being perfectly aware of the significance of the law he formulated, Vavilov 
quoted the remarkable, indeed prophetic, words of de Candolle (A. de Candolle, 
1888, La Phytographie, p. 80) who wrote, that a day will come, when science will 
interpret the elements of a species as the elements of a genus, as the 
elements of a family, and all these groups will be coordinated according to a 
definite uniform system. Vavilov was perfectly justified in his conclusion: ‘This 
day has come” (Vavilov, 1936, p. 79). 


The tropical family of arborescent plants, Dipterocarpaceae, is a good 
illustration for the ideas of Alphonse de Candolle and Nikolay Ivanovich Vavilov. 
All the taxonomic ranks of this family follow the law of homologous series that is 
common for all plants and, in fact, for all organisms. The genera of the Diptero- 
carpaceae are so closely allied to one another, that they can be regarded as initial 
species, as it were, evolved up to the generic level. 


Thus, it is not only the infraspecific systems of hereditary forms of cereals, 
legumes, Cucurbitaceae and other cultivated plants, but also the species of gigantic 
tropical trees belonging to the Dipterocarpaceae that form homologous series. As it 
is illustrated by the example of this family, the Law of Homologous series in 
Hereditary Variation is directly associated not only with the initiation of new forms 
within a species as in the case of cultivated plants, where the action of the natural 
selection is superseded by artificial selection and where many forms and varieties 
of plants therefore have good chances for survival but also with speciation. 


__ The obvious fact of the abundance of species characteristic of the genera of 
Dipterocarpoideae, particularly, of such genera as Shorea, Hopea, Dipterocarpus 


130 Gardens’ Bulletin, Singapore — XX1X (1976) 


and Vatica almost confined to the tropical rain forests of Southern and South- 
Eastern Asia should be explained. 


Earlier I assumed (Fedorov, 1966) and this provoked some criticisms in the 
botanical literature (see Van Steenis, 1969, pp. 108-109; Ashton, 1969) that in a 
tropical rain forest the abundance and diversity of species within many genera and 
families of trees is explained by the fact that there natural selection does not 
eliminate indifferent characters; these characters remain in the populations, their 
frequency being governed by genetic drift. Of these forms possessing such 
characters, those having the rank of species survive. As it becomes clear at present, 
the possibility of initiation of such characters is afforded by the law of homologous 
series: being indifferent, they are homologous to the corresponding characters that 
are useful in certain closely allied forms. Despite the abovementioned criticisms 
of my views, I am still convinced, that if the speciation in the humid tropics was 
accomplished only by means of natural selection, without participation of genetic 
drift, there too, similarly to the northern zone of the Holarctic, each genus of wild 
plants would be represented by fragmentary group of species that would not form 
any perceptible homologous series. 


One of the good examples of parallel (according to my concept, homologous) 
series, probably also formed by genotypic factors, within subgenera and other 
infrageneric taxa of the tropical genus Ficus having an extremely wide range 
(comprising about 900 species) is pointed out by E. J. H. Corner (1959, pp. 
106-108), who designated this phenomenon, after Darwin, parallel evolution. Here 
the characters pertaining to the form of inflorescences and their position on a shoot 
are subjected to parallel (homologous) variation, as well as ramiflory and cauliflory 
and also geocarpy. The forms of growth or life forms in the subgenera of the genus 
Ficus also exhibit parallel (homologous) variation manifested in all the types 
from pachycaul trees to leptocaul trees. Epiphytic species of Ficus occur in at least 
three series. Creeping forms occur in five series in various combinations with 
epiphytic. Still more diverse are the homologous forms pertaining to the structure 
and venation of leaves, as well as to their size, both relative and absolute. Corner 
(l.c.) emphasizes that there can be no doubt in the convergent origin of all these 
forms, since parallel (homologous) species of different genera differ distinctly 
from one another in the structure of flowers, by the characters of which the main 
taxonomic subdivisions of the genus Ficus are delimited. 


Corner makes an important reservation, that for instance, the case of a parallel 
(homologous) appearance of species of the genus Ficus with narrow leaves 
resembling the leaves of willow occur in the groups of the genus Ficus indigenous 
to different phytogeographical regions (Corner, 1961, p. 108; Corner, 1967, p. 33). 


The same phenomenon in different families of tropical plants had already 
been mentioned by C. G. G. J. van Steenis (1948-1954, pp. LVII-LVIII). 


As yet the mechanism of the origin of homologous series in different genera 
and families of plants in the humid tropics is not quite clear. The assumption that 
it is to a great extent based on mutagenesis leading to genotypic changes is quite 
justified, although, undoubtedly, many specific examples can also be phenotypic. 
Since allied species possess homologous characters, it is most probable that the 
genes responsible for these characters are also homologous or even identical at 
least within the same family. It was Vavilov himself (Vavilov lI.c.) who referred 
to the facts of induction of artificial mutations in species of Drosophila that followed 
the law of homologous series. 


Recombinations resulting from hybridization, serving, like mutations, as it 
were as raw material for natural selection, hardly played any significant role in 
speciation with respect to tropical trees, since hybrids occur rarely here (see Van 


Speciation in the tropics 131 


Steenis, 1969, p. 111). Chromosome numbers, for example, in different genera of 
the family Dipterocarpaceae, the object of my interest, in many cases prove to be 
the same. In most species of the genus Dipterocarpus studied (as yet not many) the 
prevailing chromosome number is 2n = 20 (see Fedorov, ed. 1969, p. 262; Moore, 
ed. 1973, p. 274). 


Corner (1954, pp. 33-34) was the first to assume that selfpollination prevails 
in the trees of tropical rain forests. Later I advanced a similar hypothesis (Fedorov, 
1966) although I overlooked Corner’s priority. Quite recently, as the result of the 
investigations of Bawa (1974), as well as of Bawa and Opler (1975) various types 
of pollination became known for both the tropical and temperate regions. By the 
way, it was revealed, that many trees apparently having bisexual flowers are 
actually dioecious in many cases, since either gynoecium or androecium prove to 
be underdeveloped, or their development proves to be asynchronous. Other details 
of the “‘reproductive biology” as it is designated by these authors and Ashton 
have been elucidated. Ashton quite recently published (Ashton, 1975, p. 109) an 
abstract of a paper on the existence, in tropical rain forest trees, of both panmixis 
and apomixis. It should be pointed out, that all the details of these phenomena in 
Tropics are as yet insufficiently studied by far, but only one fact, but a most the 
important one, should be apparently recognized to be beyond doubt: interspecific 
hybridization is a very rare event in tropical rain forests. 


Nature itself has established many almost insuperable obstacles to spontaneous 
hybridization between species of tropical trees which would lead to heterozygosity. 
This fact was mentioned in my earlier paper (Fedorov, 1966). The difficulty of 
such hybridization is, in the first place, the consequence of non-coincidence of the 
time of flowering, particularly, in the equatorial zone where there are no seasons 
of the year. This non-coincidence is observed even among individuals belonging 
to the same species, let alone those belonging to different species; another obstacle 
is the prolonged and irregular period of sterility, sometimes lasting for several 
years, then the low population density of many species, up to almost perfect 
dissociation of separate individuals of these species, i.e. their spatial isolation, and 
also biotic isolation and, in general, the diversity of biological niches. 


The survival of a large number of species belonging to the genera of Diptero- 
carpaceae and their resistance to the pressure of natural selection can be explained 
by the early development of isolation from one another of the most diverse types. 
This problem was successfully studied by P. W. Richards (1969, pp. 149-153) 
and by F. R. Fosberg, who delivered a paper on this topic at one of the symposia 
of the XIth International Botanical Congress held in Seattle (Fosberg, 1969, p. 62). 


Th. G. Dobzhansky (1950, pp. 219-221), in his study especially devoted to 
the problem of evolution in the tropics, correctly emphasizes, that in the temperate 
and in the cold zones such elementary factors as the sufficient or insufficient 
quantity of food and the degree of resistance to low winter temperatures played 
the most important rdéle in the process of natural selection. In the humid tropics 
the interrelations with the environment are more complicated; its requirements are 
more refined, while the response of organisms is more diverse and complicated; the 
role of the biotic environment is significantly more important, than in temperate 
and cold regions. 


Polyploidy, apparently, also played a certain role in the speciation in tropical 
trees. At least polyploids have been found in some species belonging to the families 
Leguminosae, Simaroubaceae, Meliaceae, Anacardiaceae, Sapindaceae, Bombaca- 
ceae, Sterculiaceae and to some other families, represented in the flora of tropical 
semideciduous forests of Costa Rica (Bawa, 1973, pp. 422-434). However, poly- 
ploid series are very rare in these cases. 


132 Gardens’ Bulletin, Singapore — XX1X (1976) 


The counts of chromosome numbers in species belonging to the genera of 
Dipterocarpaceae were commenced only quite recently. Chromosome numbers have 
been determined for only thirty species (see Fedorov, ed. 1969, p. 262; Moore, 
ed. 1973, p. 274). If it is remembered that this family comprises 580 species, it 
would be clear, that any conclusions concerning the rdle of polyploidy in the 
evolution of this family would be as yet premature. Nevertheless, the prevailing 
chromosome number being 2n = 20 (genus Dipterocarpus), cases have already 
been recorded of diverse numbers in certain species of the genus Shorea, where 
the chromosome number is 2n = 14 or 28. There are cases when 2n = 12 
(Pentacme), while in the genus Dipterocarpus rarely occur species with 2n = 30. 
The main ‘x’? numbers in different genera of the family are probably close to 
5-7-11. 

It is possible to interpret from a new point of view the phenomenon of 
convergence, which is very conspicuous and widespread in the trees of a tropical 
rain forest. This convergence pertains to the shape of leaves, inflorescences and 
other parts of plants belonging to different genera and families, particularly in the 
tropical Lauraceae, Annonaceae, Sapotaceae, Fagaceae and many others. This 
convergence is adaptive, but probably it is based on the law of homologous series 
in hereditary variation as dealt with in this paper. 


Genera Dipterocarpacearum 


A] 2] 3] 4).4 [6b | Af ting 


Homologous 
characters 
3 
oO 
OQ, 
°o 
ae 


Folia late-elliptica vix 
acuminata, obtusa vel 
retusa ca 20 cm. longa 
et 15 cm. lata 


Dipterocarpus 
+, | Vatica 
+ | Vateria 
Doona 
Parashorea 
Dryobalanops 
Cotylelobium 
Pentacme 
Monoporandra 


4. 


a 


Praeced. similia, ca 
10-15 cm. longa et 5-7 
cm. lata 


Praeced. similia, ca 


5-10 cm. longa et 3-5 


cm. lata 


Folia oblongo-elliptica 
vix acuminata, ca 
25-35 cm. longa et 
10-15 cm. lata 


Praeced. similia, ca}| + | +] +] + 
10-15 cm. longa et. 
3-7 cm. lata 


+ 
eee 
fit 


Speciation in the tropics 133 


Homologous 

characters 2 
p. 

a 

8 

7k eh s 

_— Q, —— 

ro) S| a 

o = _— 

wa bia | G 

oa 


Folia late-ovata acumi- + 
nata, ca 10-15 cm. 

longa et 6-8 cm. lata 

Praeced. similia, ca + ier b+ +/+ 
5-10 cm. longa et 3-7 

cm. lata 

Folia obovata  vix + 
acuminata, 10-20 cm. 

longa et 5-6 cm. lata 

Praeced. similia, ca + 
3 cm. longa et 2 cm. 

lata 


Folia obovata obtusa, 
ca 4.5 cm. longa et 3 
cm. lata 


Folia rotunda obtusa, + 
ca 15 cm. longa et lata 

Folia rotunda _ vix 2 
acuminata, ca 15 cm. 

longa et lata 


Genera Dipterocarpacearum 


N 
Ww 
> 
ae 
oo 
\o 
_ 
oO 
—" 
— 
— 
Ne 


Anisoptera 
Parashorea 
Monoporandra 


Vatica 


Fa el 
Ba | 
+ + + 

Cee toa | 
et ees & | | 
See ee BIT 
Bie tes Pee | po 
Ree et oP | Ss 
$5) SE Be 
Mei ae 


Folia fere rotunda vix 
acuminata, ca 3 cm. 
longa et 2.8 cm. lata 


+ 


Folia late lanceolata + + | + 

acuminata, ca 20 cm. 

longa et 5 cm. lata 

Praeced. similia, ca 7 oe + + 

cm. longa et 4 cm. lata 

Folia elliptica  apice + | + + > + 
caudata, ca 7 cm. 

longa et 3 cm. lata 


ao 


+ 


134 Gardens’ Bulletin, Singapore — XX1X (1976) 


Genera Dipterocarpacearum 


Homologous b 
characters 3 a 5 s 
ee Po ec Be = 
bel oO xs o e 
§ o ww & ro) fo) 
gia] § = | & & | 2). 8.8 0 
a a. ~ oO n 3 ° > ~~ r= 
Shoe poe «3 | a = | £2 oe 
wm im|aA >< & | Oo) Oor eee 
ms 


+ | Doona 


evber TL 
oo 
ob 


+ | Vatica 


Praeced. similia, ca 6 
cm. longa et 2-3 cm. 
lata 


Folia late ovata apice 
caudata, ca 6 cm. 
longa et 2.5-3 cm. lata 


Folia oblanceolata ob- 
tusa, ca 10-15 cm. 
longa et 4.5 cm. lata 


Praeced. similia, ca} + 
3-5 cm. longa et 1-3 
cm. lata 
SDs 
a[rmvwmme [efel [ele [=| [11 
open ae 
Sete 9S 


25 | Lamina foliorum om- 
nino glabra 
26 | Lamina foliorum plus- | + +] + + 
minusve pilosa, tomen- 
tosa vel hirsuta 
27 | Fructus magni, ca] + + + + T+ 
10-15 cm. longi 
28 | Fructus 5 Ape ca 
5-7 cm. longi 
29 mig oa parvi, ca 2-3 
cm. longi 
30 | Calycis lobi post an- 
thesin accrescentes 
Calycis lobi abbre-| + | + | + | + 
viati, fructus globosi 


Speciation in the tropics 135 


References 


ASHTON P. S. 1962. Some New Dipterocarpaceae from Borneo. Gdns’ Bull., 
Singapore 19: 253-319. 


1964. Manual of the Dipterocarp trees of Brunei State. Univ. Press, 
Oxford. 


———_——— 1967. Taxonomic notes on Bornean Dipterocarpaceae, 3. Gdns’ 
Bull., Singapore 22: 259-352. 


1969. Speciation among tropical forest trees: some deductions in 
the light of recent evidence. Biol. J. Linn. Soc. 1: 155-196. 


1975. The reproductive biology of some rain forest trees and their 
evolution. Abstract of the paper presented at the XII Internat. Botan. 
Congress, Leningrad. 


BAWA K. S. 1973. Chromosome numbers of tree species of a lowland tropical 
community. J. Arnold Arbor. 54: 422-434. 


1974. Breeding Systems of the species of a lowland tropical 
community. Evolution 28: 85-92. 


—— P. A. OPLER. 1975. Dioecism in tropical forest trees. Evolution 
29: 167-179. 


CORNER E. J. H. 1954. The evolution of tropical forest. In: J. Huxley, A. C. 
Hardy, and E. B. Ford (eds.). Evolution as a process. Allen & Unwin, 
London. 


1961. Evolution. In: A. M. McLeod and L. S. Cobley, Contem- 
porary botanical thought. Oliver & Boyd, Edinburgh. 


1967. Ficus in the Solomon Islands and its bearing on the post- 
Jurassic history of Melanesia. Phil. Trans. R. Soc. Lond. B. 253: 23-159. 


DOBZHANSKY, Th. 1950. Evolution in the Tropics. Am. Scient. 38: 209-221. 


FEDOROV, An. A. 1966. The Structure of the tropical rain forest and speciation 
in the humid tropics. J. Ecol. 54: 1-11. 


1969. (Ed.). Chromosome numbers of flowering plants. Leningrad. 


FOSBERG, F. R. 1969. The problem of isolation in the lowland tropical rain 
forest. Abstracts of the papers presented at the XI Intern. Botan. Congress, 
Seattle. 


FOXWORTHY, F. W. 1927. Commercial Timber Trees of the Malay Peninsula. 
Malayan Forest Records 3. 


1932. Dipterocarpaceae of the Malay Peninsula. Malayan Forest 
Records 10. 


MOORE, R. J. 1973. (Ed.). Index to plant chromosome numbers 1967-1971. 
1.B.P.T., Utrecht. 


RICHARDS, P. W. 1969. Speciation in the tropical rain forest and the concept of the 
niche. Biol. J. Linn. Soc. 1: 149-153. 


SLOOTEN, D. F. Van 1932, The Dipterocarpaceae of the Dutch East Indies, 6. 
The genus Dryobalanops. Bull. Jard. bot. Buitenzorg Ser. 3, 12: 1-45. 


136 Gardens’ Bulletin, Singapore — XX1X (1976) 


1940-1949. Sertulum Dipterocarpacearum Malayensium I, II, 
Il, 1V. Bull. Jard. bot. Buitenzorg, Ser. 3, 16: 430-454 (1940); Ibid. 17: 96-138 
(1941); Ibid., 17: 220-225 (1942); Ibid. 18: 229-269 (1949). 


(1952). Sertulum Dipterocarpacearum Malayensium 5. Rein- 
wardtia, 2: 1-68. 


STEENIS, C. G. G. J. Van 1948-1954. Flora Malesiana, Ser. 1, 4. 


1969. Plant speciation in Malesia, with special reference to the theory 
of non-adaptive saltatory evolution. Biol. J. Linn. Soc. 1: 97-133. 


SYMINGTON, C. F. 1943. Foresters’ manual of Dipterocarps. Malayan Forest 
Records 16. 


VAVILOV, N. I. 1920-1935. The law of homologous series in variation (in 
Russian). Saratov (1920). Idem in J. Genet. 12 (1) (1922). Idem in Theoretical 
basis of plant selection, 1 (1) (in Russian). Revised and enlarged edition by 
the author (1935). 


1930. Linnean species as a system (in Russian). Trudy po 
prikladoni botanike, genetike i selektsii 26 (3). 


WILLIS J. C. 1966. A Dictionary of the Flowering Plants and Ferns, 7th edition. 
Revised by H. K. Airy Shaw. Univ. Press, Cambridge. 


The Morphology and Systematics of Pandanus Today 
(Pandanaceae)* 


by 
BENJAMIN C. STONE 


Department of Botany, University of Malaya, Kuala Lumpur, 
Malaysia 


Summary 


More than 500 species of Pandanus are now known, and 70% of these have been 
described since 1900, nearly half since 1939, and new ones are being discovered. Many 
obstacles have prevented the completion of a monograph (dioecism, large structures, remote 
locales) but perhaps the most serious has been ignorance of morphology and morphogenesis. 
Studies of these are thus of critical importance. Micromorphological-anatomical data and 
cytotaxonomic data have recently become available, permitting data integration not previously 
possible, This has resulted in a new detailed infrageneric classification which can contribute 
to understanding of the phylogeny. This classification recognizes 8 subgenera, 62 sections, 
and 22 subsections covering 468 species and numerous synonyms. Chromosome numbers 
are 2n = 60 (1 species of Pandanus, P. spiralis R. Br., has 2n = c. 120). Remarkable stomate 
variability is tied almost exclusively to systematic relationship. 


I. Introduction 


The Pandanaceae is a family now generally conceded to be the sole member 
of the Order Pandanales (Monocotyledonae). The Typhaceae and Sparganiaceae 
(formerly included) are not closely related to Pandanaceae and form a distinct 
Order Typhales. 


Although known to botanists for some three centuries, the Pandanaceae 
accounted for in Warburg’s Monograph (1900) were 180 species of Pandanus, 
about fifty spp. of Freycinetia, and one of Sararanga. No further genera have been 
discovered but the number of known species has grown and there are about 700 
binomials currently, The foremost students of the family since 1900 have been 
Martelli, Merrill, Pichi-Sermolli, and St. John. More vigorous exploration in the 
Palaeotropics has vastly increased the available study material; much fieldwork 
has significantly augmented the herbarium study. 


But many problems remain which impede full understanding of the family, 
in particular the largest genus Pandanus. With over 500 species, Pandanus posed 
severe difficulties in establishing interspecific relationships and an infrageneric 
classification. 


II. Traditional taxonomic characters and unresolved problems 


The salient features of previous taxonomic work on Pandanus was the virtually 
complete dependency on the characters of the ripe fruits. Nearly all described 
species and infrageneric taxa were based on fruit-characters. Since all the plants 
are dioecious, this resulted in almost sure ignorance of the males. Staminate 
specimens could seldom be identified. The problem was brought about by the 


* Based on a paper read at the International Botanical Congress at Leningrad, 1975 
(Abstract in [A. Takhtajan (Ed.),] Abstracts of the papers presented at the XII International 
Botanical Congress July 3-10, 1975 (1):100). 


137 


138 Gardens’ Bulletin, Singapore — X XIX (1976) 


rarity of good staminate material in herbaria (in turn the result of the ephemeral 
nature of the male flowers in nature), and the difficulty of correlating staminate 
and pistillate specimens both in the field and in the herbarium. Sterile material 
was impossible to identify. 


Clearly, a taxonomic system which relied entirely on fruit characters, in a 
genus of strictly dioecious plants, was inadequate both for practical identification 
and for studies of phylogeny. For the purposes of most botanists, identification of 
Pandanus was either uncertain or impossible. 


In view of this situation it was obviously desirable to seek taxonomic 
characters which were shared by both staminate and pistillate plants, i.e. vegetative 
characters, including those revealed by micromorphology and anatomy. During the 
past two decades our efforts have been turned to solutions to the problems 
described. The main features of the work, carried out by various persons at several 
institutions, are described below. 


III. New Investigations and their Results 


A. Gross Morphology. — In general three main aspects have been developed: 
(1) Fuller quantification of characters, particularly of vegetative structures. 
Example: the mainly qualitative descriptions of leaves have been replaced by 
analyses giving data such as tooth (prickle) size and spacing, vein number, 
variation in leaf length and width, etc. (2) The discovery and correlation of 
staminate with the pistillate-plants of the same species, and full descriptions and 
taxonomic use of staminate characters. Example: field work yielding field know- 
ledge of population structure, phenology, breeding behaviour, and ecological 
distribution, has often led to correct correlation of sexes. Pollen characters have 
been studied only to a limited extent but may throw some light on species relation- 
ships, as has been demonstrated in a few cases (e.g. Pandanus sigmoideus St. John). 
(3) Habit and morphogenetic field characters supplementing the existing herbarium 
knowledge, made possible by augmented collection techniques, photography, field 
analysis of individuals in various growth stages, etc. 


B. Morphogenesis and architecture (habit). — Work in this field has revealed 
the changes which occur in ontogeny from seedling to adult and has necessitated 
the recognition of ‘juvenile’ states which may differ radically from adult states, 
even in the same species. Progressive changes in anatomical features are correlated 
with the external changes in size and form, and indicate that anatomical characters 
must be derived from adult structures for reliable use in taxonomy and classifica- 
tion. Habit classification has become possible through the analysis of growth phases 
and it is now clear that adult form can be a major taxonomic character, This is 
especially clear in the case of Pandanus Sect. Acanthostyla, of Madagascar, a group 
of species which share the ‘coniferoid’ habit. Further studies of habit have been 
carried out by Guillaumet (1973), based on the more general work of Hallé and 
Oldemann (1970; 1975). The ‘lateral’ inflorescences of Sect. Cauliflora and Sect. 
Tridens are similar examples of habit specialization which offer taxonomic utility. 


C. Anatomy. — Anatomical studies of Pandanus date back at least as far as 
Solla (1887) but their significance in relation to taxonomy was not appreciated. 
With resumption of such studies by Tomlinson (1965), Kam (1969), Gineis 
(1969), and now especially by K. L. Huynh (1974), the correlation between — 
anatomical features and other characters became clear. It is now evident that, in — 
general, anatomical characters form a fairly reliable basis for the discrimination 
of species-groups, and furthermore, it has become clear that these species-groups 
usually correspond to sections. Occasionally, single species stand out on anatomical 
grounds, and there are_some cases in which anatomy seems not to offer clear 
support to sectional discrimination, but in a great majority of cases the anatomical 
data has had a beneficial and significant effect on infrageneric taxonomy. The 


Pandanus, Morphology and Systematics 139 


anatomical characters used have been chiefly from the leaves, and as demonstrated 
by Kam, only fully adult organs could be compared. Within these limits the 
appearance of particular anatomical features seems sufficiently constant and in rare 
cases may be diagnostic. 


The tissues which furnish the characters are especially the epidermis, the 
stomatal complex, the hypodermis, the crystal cells, the chlorenchymatous layers, 
the fibrous strands and the vascular bundles. In particular, the range of variation 
in the epidermal tissues (including the stomata) proves to be of very great value. 
In order to rationalize the variation found, Tomlinson founded a classification of 
stomatal types, based on progressive complexity. This system was used by Kam 
and others and shown to correlate well with sectional taxa. More recently (1974) 
the classification has been refined by Huynh, who defines seven stomatal types and 
in turn finds a remarkably good correspondence with the infrageneric classification 
being developed by Stone. In fact, the anatomical data became the test by which 
the infrageneric taxa could be evaluated; where serious disharmony in anatomical 
features was revealed within a section, it was usually found to indicate an artificial 
classification which could be remedied by remodeling the Section e.g. by dividing 
it, or by reassigning some of its supposed component species to other sections. The 
anatomical data thus often revealed a ‘hidden’ flaw in previous taxonomic systems. 


Examples of the variety of stomatal-complex structures revealed that all retain 
the basic tetracytic pattern but vary in relation to the production of elaborations, 
which are commonly in the form of papilliform protuberances arising from the 
cells of the stomatal complex and of the epidermis proper. The simplest arrange- 
ment is an essentially flat epidermis, the stomate flush with the surface, the 
epidermal cells merely forming a tessellate pattern. On adaxial surfaces of leaves 
the epidermis may be zoned or not; zonation involves differing cell shape and 
presence or absence of stomata in alternating bands corresponding to veins and 
inter-vein spaces. Such zonation produces a further character that may be used in 
addition to the stomatal type. Increasingly complex stomatal types develop as 
various cells produce papillae, and the entire epidermal surface or all the relevant 
zonal bands, may thus become papilliferous. The papillae themselves may be 
limited to one per cell, or may occur in sets on a cell: they may be of various 
simple forms or in more elaborate forms such as forked or dendritic. Papillae may 
form a stockade around the stomate, or around a group of stomata. The stomata 
may become considerably sunken below the general level of the epidermis. 


The hypodermis may be of one or more cellular layers and may include 
crystal cells in various patterns and in various orientations. The crystals may be 
trhomboidal or occur as raphides; the former usually are more common in leaves, 
and may exist in two distinct forms, and in various sizes. The patterns of distribu- 
tion of the crystal cells may be of some taxonomic value. 


The chlorenchyma may be continuous or interrupted, and this distinction 
sometimes has a taxonomic significance. 


The association of fibrous strands with particular tissues may also be constant 
enough for taxonomic use. 


A considerable number of other anatomical features occur, some of which 
may on occasion have a taxonomic use, e.g. stomatal size and stomatal index, the 
occurrence of papillate stockades, etc. 


Wherever data from anatomy conflicts considerably with a traditionally 
established taxonomic group it is likely that the latter is heterogenous and a 
re-evaluation of all the constituent species and their characteristics is in order. By 
application of this method the infrageneric classification can be established on a 
broader, firmer basis than otherwise possible. The concrete result of such applica- 
tion has been put forward as a new infrageneric scheme (Stone, 1974). In this 
system, eight subgenera are established (these are further grouped into four 


140 Gardens’ Bulletin, Singapore — X XIX (1976) 


unnamed groups of 3, 2, 2 and 1 subgenera respectively). Each subgenus consists 
of one or more (up to sixteen) sections. Altogether, 62 sections are recognized. 
These in turn are in some cases divided into subsections, There are 468 species 
accounted for, i.e. probably 90% of the total (the remainder are excluded 
temporarily as either probable synonyms or because data is quite insufficient for 
placement). 


D. Cytology. — The predominant chromosome number found in Pandanus 
is 60 (somatic): but one tetraploid (P. spiralis R. Br.) is known. However, 
only some 30 species have been ‘counted’. The foremost workers in this field 
have been Tyjio, Harada, Cheah (1969) and the work is being continued by Jong. 
The only discovery of some taxonomic significance is that in some cultivars (e.g. 
P. spurius Miq.) some cells at least may be aneuploid (with such numbers as 59 
or 61 chromosomes). So far however, there is no significant input from chromosome 
studies, but the work has probably not progressed far enough to be sure that this 
will remain true. It is at least potentially interesting that the one case of tetraploidy 
occurs at the margin of the generic distribution (Northern Territory, Australia) 
where it seems to be the case that habitat and climatic conditions are marginal. 
The karyotype analysis by Cheah shows that the chromosomes are very small. 
There may be 0-4 pairs of SAT-chromosomes, and many are short rods which are 
hardly discriminable, 


E. Embryology. — Pandanus is peculiar in that the mature embryo sac in 
the few species so far studied, has a condition of supernumerary nuclei (over and 
above the usual eight): these nuclei, as was shown by Fagerlind (1940), migrate 
in from the surrounding tissue at a late stage. Recently this has been reconfirmed 
in two Malayan species (Cheah and Stone, 1975). The other genera of the family 
do not appear to show this phenomenon. The significance, if any, to taxonomy, 
has yet to be discovered. However, circumstantial evidence for a few species 
indicates that reproduction may be apomictic: it is conceivable that this is related 
to the ‘nuclear migration’ as first noticed by Campbell and demonstrated by 
Fagerlind, but this remains to be investigated. 

F. Palynology. — The pollen morphology has yet to be investigated in detail. 
Present evidence suggests that some variation exists and thus some taxonomic 
information may arise from studies of pollen. It is hoped to investigate this with 
the Scanning-Electron Microscope now available in the University of Malaya. 


IV. Synopsis of the infrageneric taxa of Pandanus' 


Group 1 
Subgenus 1. Rykia 
Sections: 
(1) Rykia (with subsec- (2) Asterodontia (7) Kaida 


tions Rykia, Bidens, (3) Hombronia 
Malaya, Multispina, (4) Mydiophylla 
Calcicola, Atroden- (5) Rykiopsis 


tata, Gressittia) (6) Solmsia 
Subgenus 2. Lophostigma 
Sections: 
(1) Lophostigma (7) Perrya (13) Bernardia 
(2) Megastigma (8) Cauliflora (14) Asterostigma 
(3) Karuka (9) Barrotia (15) Tridens 
(4) Maysops (10) Liniobtutus (16) Cheilostigma 
(5) Metamaysops - (11) Brongniartia 


(6) Paralophostigma (12) Veillonia 


1. See Stone (1974) for bibliographic citations. 


Pandanus, Morphology and Systematics 


Subgenus 3. Kurzia 
Sections: 

(1) Kurzia 

(2) Microstigma 

(3) Jeanneretia 

(4) Pulvinistigma 


Subgenus 4. Vinsonia 
Sections: 
(1) Vinsonia 
(2) Barklya 
(3) Mammillarisia 
(4) Dauphinensia 
(5) Stephanostigma 


141 


(5) Curvifolia 
(6) Involuta 
(7) Marginata 
(8) Cristata 


(9) Kanehiraea 
(10) Utilissima 


Group 2 


(6) Heterostigma (9) Acanthostyla 
(7) Souleyetia with (10) Rykiella 
subsections Souleyetia (11) Lonchostigma 
and Sussea (12) Platyphylla 
(8) Foullioya (13) Eydouxia 


Subgenus 5. Martellidendron 


Sections: 
(1) Martellidendron 


Subgenus 6. Pandanus 
Sections: 

(1) Pandanus, with Sub- 
sections Pandanus, 
Austrokeura, and 
Insulanus 

(2) Fagerlindia 

(3) Elmeria 

(4) Athrostigma 


Subgenus 7. Coronata 
Sections: 
(1) Coronata 


Subgenus 8. Acrostigma 
Sections: 

(1) Acrostigma, with 
Subsections 
Acrostigma, 
Scabridi, 
Dimissistyli, 
Ornati, 


Y. Future work needed. 


(2) Seychellea 


Group 3 


(5) Intraobtutus 
(6) Australibrassia 
(7) Semikeura with 
Subsections 
Semikeura and 
Elaphrocarpus 
Excavata 


(9) Megakeura 


(8) 


Group 4 


Glaucophyllae, 
Parvi, 
Papilionati, 
Alticolae, and 
Pumili 

(2) Fusiforma 


(3) Pseudacrostigma 
(4) Epiphytica 


A. Functional significance of micromorphological-anatomical characters: The 


great variation in anatomical structure which correlates so well with classification, 
seems so far to resist an ecological or physiological explanation. For example, the 
more elaborate stomatal types (five in Tomlinson’s, six or seven in Huyhn’s) 


142 Gardens’ Bulletin, Singapore — X XIX (1976) 


suggest xeromorphy. Nonetheless, various species of Pandanus which are taxono- 
mically unrelated and which have very different stomatal types, may occur 
sympatrically in exactly the same microhabitat, i.e. fresh-water swamps. 

B. More precise developmental studies to determine the basis of different 
habit categories, as well as to provide a means to compare ontogeny in pandans 
with that in other plants. 

C. Further cytological studies to determine if other examples of polyploidy 
exist, whether they correlate with classification and/or habitat, and whether they 
tend to cluster at the margin of the generic distribution as is apparently the case 
and would be expected theoretically on the basis of the evolutionary studies of 
e.g. Stebbins. 

D. Palynological work as a basic survey and to correlate with taxonomy and 
with fossils, particularly to see whether palynomorphic form genera such as 
Pandaniidites can be in fact accepted as pandanaceous. 


E. Distributional analysis as a partial basis of phylogenetic interpretation. 


References 


CHEAH, C. H. 1969. M.Sc. thesis, University of Malaya. 


———— 1973. Chromosome studies of Pandanus. Bot. Jahrb. Syst. 93: 
498-529. 


——— & B. C. STONE. 1975. Embryo sac and microsporangium 
development in Pandanus. Phytomorphology 25: 228-238. 

FAGERLIND, F. 1940. Stempelbau und Embryosackentwicklung bei einigen 
Pandanazeen, Annls Jard. bot. Buitenz. 49: 55-78. 


GINEIS, C. 1969. Etude anatomique de la plantule de Pandanus sp. Bull. Inst. 
Fr. d’ Afr. noir 31 A, 2: 325-339. 

GUILLAUMET, J.-L. 1973. Formes et development des ‘Pandanus’ Malgaches. 
Webbia 28: 495-519, 6 figs., 10 pls. 

HALLE F. & R. A. A. OLDEMAN. 1970. Essai sur Il architecture et la 
dynamique de croissance des arbres tropicaux. Masson & Co., Paris. 

1975. Essay on the Architecture and Growth Dynamics of Tropical 

Trees. English translation by B. C. Stone. University of Malaya Press, Kuala 
Lumpur, 

HUYNH, K. -L. 1974. La morphologie microscopique de la feuille et la taxonomie 
du genre Pandanus. Bot. Jahrb. Syst. 94: 190-256. 


KAM, Y. K. 1969. M.Sc. thesis, University of Malaya. 
1971. Morphological studies in Pandanaceae III. Comparative 


systematic foliar anatomy of Malayan Pandanus. Bot. J. Linn. Soc. 64: 
315-351. 


& B. C. STONE. 1970. Morphological studies in Pandanaceae IV. 

Stomate structure in some Mascarene and Madagascar Pandanus and its 
meaning for infrageneric taxonomy. Adansonia n.s. 10: 214-246. se 
SOLLA, R. F. 1884. Contribuzione allo studio degli stomi delle Pandanee. Nuovo — 
G. bot. ital. 16: 172-182. | 
STONE, B. C. 1974. Towards an improved infrageneric classification in Pandanus 
(Pandanaceae). Bot. Jahrb. Syst. 94: 459-540. 
TOMLINSON, P. B. 1965. A study of stomatal structure in Pandanaceae. Pacif. 

Sci. 19: 38-54, _. 


WARBURG, O. 1900. Pandanaceae, in A. Engler, Das Pflanzenreich, 3, IV. 
9: 1-97, Engelmann, Leipzig. 


Ternstroemia corneri (Theaceae) 
by 
HsuAN KENG 


Department of Botany, University of Singapore 


In preparing a systematic account of the Malayan Theaceae for volume 3 of 
the Tree Flora of Malaya, I came across an obviously undescribed species of Tern- 
stroemia from southern Johore. It is represented by several specimens collected 
by Professor E. J. H. Corner and others, all deposited at the Herbarium of the 
Botanic Gardens, Singapore, of which one (Corner SFN 27840) was sent to Kew 
as early as 1935 for identification and returned with an annotation sheet stating 
that it was “‘Not matched in Kew’’, signed by Mr. Fisher in 1936. Its large, obovate 
or oblanceolate leaves and ellipsoid fruits with a pointed apex are so characteristic 
that it can be readily differentiated from other large-fruited Ternstroemia species 
of Malaya and indeed those of the rest of the Malaysian region. The new species, 
dedicated to Professor Corner, is described below. 


Ternstroemia corneri H. Keng, sp. nov. 


Arbor 12-20 metralis, ramulis teretibus. Folia coriacea, auguste obovata vel 
oblanceolata, 20-28 cm longa, 7-8.5 cm lata, apice rotundata vel mucronata, basi 
longa attenuata, margine integerrima, nervis 13-15 paribus; petiolis circa 1 cm 
longis, incrassatis. Flores solitarii, proxime positi, pedicellis 2—2.5 cm_longis, 
bracteolis 2, suboppositis, lineo-lanceolatis, 5 mm longis, sepala 5-6, obovato- 
rotundata, 5-6 mm longa, petala 5—6, oblongo-obovata, 8-10 mm longa; stamina 
numerosa (circa 80), 5-7 mm longa, ovarium conicum, 2-4 mm longum, 2-loculare, 
loculis 2 plusve ovulatis. Fructus ellipsoideus vel auguste ellipsoideus, 4.5-5 cm 
longus et 2—2.5 cm diametro, seminibus 2-4. 


Small to medium-sized tree, 12-20 m tall. Bark greyish, no stilt roots or 
buttresses. Branches and branchlets terete. Leaves 3-4 in a false whorl, coriaceous 
or thin coriaceous, narrowly obovate or oblanceolate, 20-28 x 7-8.5 cm; lateral 
veins 13-15 pairs; apex rounded or abruptly and bluntly mucronate; base long- 
attenuate; petiole 1 cm long, stout. Flowers solitary, in axils of fallen leaves, 
2-2.5 cm across if fully expanded, peduncles 2-2.5 (—3) cm long; bracteoles 2, sub- 
opposite, a short distance below the calyx; sepals 5-6, obovate-rounded, 5-6 mm 
long; petals 5-6, oblong-obovate, 8-10 mm long; stamens about 80, in 3-4 series, 
the connective produced and pointed; ovary conical, 2-4 mm long, 2-loculate, with 
2 ovules per locule, the style 2-forked. Fruit baccate, ovoid or narrowly ovoid, 
4.5-5 cm long, 2—2.5 cm in diameter, seeds 2-4, ellipsoid, flattened. 


Known only from southern Johore, Peninsular Malaysia, in lowland swamp 
forests. 


Specimens examined: Johore, Sungei Berassau, Mawai-Jemuluang Road, 
Corner SFN 28740 (Type) (in swamp forest), 6 February 1935; Sungei Sedili, 
Corner s.n. in March 1932 (a tree, up to 50 feet); Mawai, Corner SFN 30888 (60 
feet, leathery leaves, yellowish green beneath); Sungei Kayu, Kiah SFN 32158; 
Sungei Kayu, Mawai-Jemuluang Road, Corner SFN 32245; Mawai, Nagadiman 
SFN 34736; Sungei Gambut, Corner SFN 36815 [all SING!]. 


143 


144 Gardens’ Bulletin, Singapore — XX1X (1976) 


A simple dichotomous key to the four Peninsular Malaysian Ternstroemia 
species with larger flowers (over 1.5 cm across) and larger fruit (over 2 cm long) 
follows: 


1. Normal leaves over 20 cm long; mature fruit distinctly ellipsoid and attenuate 
toward both ends, over 4.5 cm Jong ...............ccceeeee eee eees T. corneri H. Keng 


1. Normal leaves less than 15 cm long; mature fruit rounded or ovoid, less than 
3.5 cm long 


2. Flower (and fruit) stalk slender, 3.5-4 cm long; leaves elliptic obovate, 
12-18 x.6-8 CM) i siaiventionitn.- pe a eee T. penangiana Choisy 


2. Flower (and fruit) stalk stout, 1-1.5 (-2) cm long, 


3. Bracteoles immediately below and clasping the calyx; mature fruit 
ovoid-rounded, 3-3.5 x 2.5-3 cm; leaves elliptic to narrowly elliptic, 
8-11 x0235-5.5. €m \2.208:5). aad. ZW. Se T. bancana Miq. 


3. Bracteoles a short distance away and free from the calyx; mature fruit 
rounded, 2.5-2.75 cm across; leaves narrowly elliptic, 12-16 x 3.5-5 
os Pert: eer eters Peet Firs ce rhe oe po T. wallichiana Engler 


I am grateful to the Director of the Botanic Gardens, Singapore, for the 
herbarium and library facilities kindly provided and to Mr. D. Teow for the 
photographs reproduced in this paper. 


Facing plate: Ternstroemia corneri H. Keng 
A branch with unfolded flowers (type, eres SFN 28740). Upper inset: fruits cut into 
halves showing the seeds (Ngadiman SFN 34736); lower inset: dissected flowers(type). 
All scales in cm. 


R CENTIMETRES 


N 
% 


ag 


#9 


CMG 


WALAY PENINSULA, 


GE JBAGRE. 


SMLNZE 


i 


jn 


coo 


Thelypteridaceae Allied to Phegopteris in Malaya 


by 
R. E. HOLTTUM 


Royal Botanic Gardens, Kew 


Summary 


Following the revised scheme of genera in the family Thelypteridaceae proposed by the 
author in 1971, a revised account is here given of the genera Macrothelypteris, Pseudophego- 
pteris and Metathelypteris in Malaya; these three genera, together with Phegopteris (sensu 
Ching 1963) appear to form a natural group. Some corrections to the nomenclature of the 
author’s book Ferns of Malaya (1955) are made, with revised descriptions where necessary, 
and the addition of two species Metathelypteris decipiens (Clarke) Ching and M. flaccida (B1.) 
Ching, not previously recorded for Malaya. 


In my book on the ferns of Malaya (1955) I described 46 species of the family 
Thelypteridaceae, but (as stated on p. 236) no natural delimitation of genera had 
then been devised; those adopted were genera of convenience. It was clear to me 
that much more detailed observation of plants throughout the oriental tropics was 
necessary before a better arrangement of genera could be found. Subsequently 
R. C. Ching (1963) and K. Iwatsuki (1963-65) proposed new systems of classifica- 
tion, but both were mainly based on species of mainland Asia, whereas the family 
is far more diversified in the Malayan region and the Pacific. For the past eight 
years I have devoted most of my time and thought to a study of the family through- 
out the Old World, including Africa, with a glance also at the New World where 
A. R. Smith of Berkeley is attempting a similar survey. In 1971 I arrived at a new 
system of genera in the Old World, based on Ching’s scheme but with considerable 
extensions. Since then I have prepared a series of monographs covering all species 
of individual genera; the series is not yet complete. 


My present estimate is that Malaya has at least 54 species belonging to the 
family; this is about 10% of the total number of species in the Old World, with 
representatives of most of the genera; most of the missing genera have their main 
distribution in mainland Asia, but one of them is Amauropelta which is mainly 
American and extends across Africa to the Mascarene Islands. 


The object of the present paper is to give a revised account of the Malayan 
species of a small group of genera which are distinguished by the following com- 
bination of characters which was first recognized by Ching: midrib of pinnae 
prominent but not grooved on the upper surface, and veins not reaching the margin. 
They also agree in having sori mainly exindusiate, and all genera except Phegopteris 
have some species with amply bipinnate fronds; such fronds do not occur in other 
genera of the family. I judge that the four genera form a natural group; if anyone 
wished to unite them, they would collectively bear the generic name Phegopteris 
(which in the strict sense of Ching does not occur in Malaya), but I prefer to 
maintain them as separate genera. They differ cytologically as follows: Phegopteris 
n = 30; Macrothelypteris and Pseudophegopteris n = 31; Metathelypteris n = 35. 
These numbers are based on several counts of plants from different sources, and of 
more than one species, in each case. Thus Metathelypteris has the same chromo- 
some number as Thelypteris s.str., but the two groups differ in many ways and are 
certainly not closely related. Phegopteris has three species, two of them widely 
distributed in north temperate latitudes, one in southern China, extending to Tonkin 


145 


146 Gardens’ Bulletin, Singapore — XX1X (1976) 


and Taiwan, with only one Malesian record, in Celebes; I found it to be easily 
maintained in cultivation at Penang, but it did not propagate itself from spores. 


The name Phegopteris derives from Polypodium phegopteris Linn. It was first 
used as a generic name to distinguish terrestrial ferns which have exindusiate sori 
resembling those of Polypodium, and was used in the 19th century to cover various 
different groups of such ferns. The present limitation of the genus is due to Ching 
(1963: 312). Its distinctive characters are: stipe-scales with marginal acicular hairs 
but no such hairs on the surface; fronds simply pinnate, pinnae connected by a 
wing along the rachis, the wing forming semicircular lobes between pinnae. 


In the following statement I have not attempted to give a full synonymy for 
each species, but I do give the following in all cases: (a) the basionym; (b) the name 
used in my book of 1955; (c) names used in conjunction with previous descriptions; 
(d) the correct name in Thelypteris, if such has been published. A full synonymy 
for Pseudophegopteris and Macrothelypteris will be found in my paper of 1969 
cited below; it will be given for Metathelypteris when I prepare a monograph. 


KEY TO THE GENERA IN MALAYA 


Fronds simply pinnate; sori distinctly indusiate ..................... 1. Metathelypteris 
Fronds mostly bipinnate; sori exindusiate or with very small indusia: 


Slender spreading acicular hairs consisting of several cells, abundant on lower 
surface of axes of frond; spores with a very fine raised reticulum not distinguish- 
able ‘with’ light ‘micrOscope’ soc dak we uatec tok sc cores tose eee 2. Macrothelypteris 


Hairs on lower surface all unicellular; spores with a slightly raised surface reticulum 
of: rather large: meshes.iu.2 07. hand. bas oad am te dor 3. Pseudophegopteris 


1. Metathelypteris Ching 1963: 304. Holttum 1971: 26 


Rhizome short, suberect. Fronds simply pinnate with deeply lobed pinnae (in 
two non-Malayan species bipinnate); veins often forked, not reaching margin; hairs 
on lower surface acicular or capitate, always unicellular; sori indusiate; no hairs or 
glands on body of sporangia. 


Distribution: about 14 species, widely distributed but few of them anywhere 
abundant; San Thomé and Fernando Po; Madagascar; Ceylon; N.E. India to China 
and Japan; throughout Malesia on mountains; Solomon Islands. 


Specimens from the islands of the Gulf of Guinea have been identified with 
the Madagascan M. fragilis (Bak.) Holtt. but may represent a distinct species. No 
specimens have been reported from Madagascar since the original specimen, a 
single frond, reached Kew in 1877. Another specimen, still undescribed and possibly 
originating from Nigeria, is the only evidence that plants of this genus now exist 
in mainland Africa. Only one species of the genus was described in Holttum 1955; 
two more are here added. 


KEY TO THE MALAYAN SPECIES 


Lobes of at least the lower pinnae lobed half-way towards costules or more deeply 
tre yine magne nae sagen’ Heine <opeieide nienmuiice~ Tarsxismeuunaame tana nan nen 1. M flaccida 


Lobes of pinnae entire or crenate: 


Pinna-lobes (except basal acroscopic lobe) entire; pinnae commonly to 6 x 2 cm; 
veins often simple in smaller pinna-lobes ..............s0+cseeeeeeeeees 2. M. decipiens 


Pinna-lobes of large pinnae crenate; pinnae commonly larger; almost all veins 
POT ooo occ cncceecens cence ee epee eeswisseveasipnayuniinellig ie Uns simnnIeInnnn 3. M. dayi 


T hely pteridaceae 147 


1. Metathelypteris flaccida (BI.) Ching 1963: 306. 


Basionym: Aspidium flaccidum Bl., Enum. Pl. Jav. (1828) 161. Racib. Fl. Btzg 1 
(1898) 176. 


Synonyms: JLastrea flaccida Moore, Ind. Fil. (1858) 92. Bedd. Ferns 
S. India (1864) t.250; Handbook (1883) 244. — Dryopteris flaccida (Bl.) O. Kuntze, 
Rev. Gen. Pl. 2 (1891) 812. v.A.v.R., Handb. Mal. Ferns (1908) 195. — Thelypteris 
flaccida (Bl.) Ching, Bull. Fan Mem. Inst. Biol. 6 (1936) 336. 


Rhizome short, erect. Stipes to 25 cm or more long, pale, hairy in the groove; 
basal scales 3-4 mm long. Lamina 25 cm or more long, with rather widely-spaced 
subopposite pinnae, to 10 pairs, thin; basal pinnae narrowed towards base on basi- 
scopic side. Largest pinnae of Malayan specimens 10 x 2.5 cm, acuminate, lobed 
almost to the costa; largest lobes lobed 4 way to costule or more deeply; costules 
to 4 mm apart; veins pinnate in the larger lobules of pinna-lobes, distal veins 
forked; lower surface of rachis, costae, costules, veins and surface of lamina bearing 
slender pale erect acicular hairs to } mm long; upper surface of costules and veins 
bearing scattered hairs as those on costa. Sori 1-3 in each lobule of a pinna-lobe, 
small; indusia thin with short acicular hairs. 


Distribution: West Java (type); Sumatra (?); Malaya; Ceylon & S. India; N.E. 
India to West China. 


In 1969 I found plants of this species on sheltered earth banks by a road at 
5000 ft near Brinchang, Cameron Highlands; specimens were also collected some- 
what earlier by Abdul Samat bin Ali (no. 363) on Maxwell’s Hill, Perak. The 
Malayan specimens are all rather small and have shorter hairs on the lower surface 
than those from Java and from N.E. India. Prof. Manton found that in Ceylon 
the species occurs in both diploid and tetraploid forms (Phil. Trans. R. Soc. B, 
238:137. 1954). Herbarium specimens from Ceylon at Kew can be separated into 
those with longer and with shorter, less abundant hairs on lower surface; the 
Cameron Highlands specimens correspond with the latter. It seems likely that this 
species will spread in northern Malaya as clearing provides suitable habitats. 


2. Metathelypteris decipiens (Clarke) Ching 1963: 306. 


Basionym: Nephrodium gracilescens (Bl.) Hook. var. decipiens Clarke, Trans. 
Linn. Soc. Il, Bot. 1 (1880) 514, t.65, fig. 2. 


Synonyms: Lastrea gracilescens var. decipiens Bedd., Handb. Suppl. (1892) 51. — 
Thelypteris decipiens Ching, Bull. Fan Mem. Inst. Biol. 6 (1936) 335. 


Rhizome short-creeping or suberect with fronds closely tufted at its apex. 
Stipe 15-25 cm long, pale except for darkened base, very-short-hairy; scales narrow, 
2 mm long, bearing short hairs. Lamina to 30 cm long, with about 12 pairs of free 
pinnae; basal pinnae sometimes a little reduced, often narrowed at the base on 
basiscopic side; texture thin. Largest pinnae on Indian specimens 9 X 2.5 cm, 
commonly 6 x 2 cm, on Malayan specimen 5 x 1.3 cm, short-acuminate with 
upcurved tip, lobed almost to costa; basal acroscopic lobe often enlarged and 
crenate, other lobes entire, slightly oblique, hardly falcate; costules to 3} mm apart; 
veins to 6 pairs, those in acroscopic basal lobes mostly forked, in other lobes mostly 
simple; lower surface of rachis, costae and costules bearing scattered short hairs, 
also short brown linear scales; upper surface of costae densely hairy, scattered 
similar hairs on costules and veins. Sori medial or a little supramedial; indusium 
small, pale, with minute capitate hairs. 

Distribution: Darjeeling district; Khasia Hills in Assam; in Malaya only found 


once on rocks in opening of mossy forest, by waterfall, Gunong Batu Brinchang, 
6000 ft (Molesworth Allen 5005). 


148 Gardens’ Bulletin, Singapore — XX1X (1976) 


This species is very near M. gracilescens (Bl.) Ching, differing in broader 
pinna-lobes of the largest fronds, with acroscopic basal lobes enlarged and crenate, 
and in having some veins forked in the larger pinna-lobes. The Malayan plant 
matches specimens from the Khasia Hills very closely; it is not mentioned in the 
appendix to the second edition of my book. M. gracilescens (type species of the 
genus) has a wide distribution on mountains in the Malayan region (Sumatra, Java, 
Borneo, Philippines, New Guinea) also Taiwan and southern Japan; it has not yet 
been found in Malaya. 


3. Méetathelypteris dayi (Bedd.) Holttum 1976: 117. 

Basionym: Nephrodium dayi Bedd., Journ. Bot. 25 (1887) 323. 

Synonym: Lastrea dayi Bedd., Handb. Suppl. (1892) 54. 

Misapplied name: Thelypteris singalanensis sensu Holttum 1955: 243, fig. 138. 


I have no corrections or addition to the description of 1955, but here provide 
a correction of the name. The type of Nephrodium singalanense Bak. represents a 
Sumatran species distinct from the Malayan one; it has abundant minute capitate 
glandular hairs all over the lower surface and the fronds are thinner in texture, 
drying a darker green. It may be a forest plant, whereas the Malayan M. day 
grows in rather open places, not in full forest shade. A plant from Taiping Hills 
investigated by Prof. Manton proved to be tetraploid; the Sumatran M. singalanensis 
might be diploid. 


Distribution: Sumatra, Malaya, West Java, Borneo, Philippines, New Guinea. 


2. Macrothelypteris Ching 1963: 308. Holttum 1969: 25 


Rhizome short, prostrate or suberect; scales at base of stipes narrow, thickened 
near their bases, with short acicular or capitate marginal and superficial hairs; 
fronds amply bipinnate-tripinnatifid with adnate pinnules; scales on rachis (if 
present) often with thickened bases, sometimes with marginal hairs, always with an 
acicular hair-tip, usually grading to septate hairs on distal parts of frond; sori small, 
with small indusia obscured by ripe sporangia; sporangia bearing capitate hairs; 
spores with a very fine surface-reticulum not distinguishable in detail with the 
light microscope, sometimes with slight wing-like outgrowths. 


Distribution: about 9 species, from the Mascarene Islands to warmer parts of 
mainland Asia, throughout Malesia, widely in the Pacific. In Malaya only one 
species, which needs no new description but has an earlier name than that cited 
in Holttum 1955. 


Macrothelypteris torresiana (Gaud.) Ching 1963: 310. Holttum 1969: 27. 
Basionym: Polystichum torresianum Gaud. in Freycinet, Voy. Bot. (1824) 333. 
Synonym: Thelypteris torresiana (Gaud.) Alston, Lilloa 30 (1960) 111. 

Name in Holttum 1955: Thelypteris uliginosa (Kunze) Ching. 


This species is at once distinguishable by its glaucous stipe with dark narrow 
basal scales and by the presence of slender acicular hairs more than 1 mm long 
and consisting of several cells, which take the place of scales on the lower surface 
of axes of the frond. It is distributed almost throughout the range of the genus and 
has also become established through human agency in various parts of the American 
tropics. It is not a common species in Malaya, except in the north, in open places 
in the lowlands, though easy to cultivate in Singapore. 


T hely pteridaceae 149 


It would not be surprising if M. multiseta (Baker) Ching, described from 
G. Matang near Kuching, Sarawak, and occurring at c. 3000 ft in the Padang High- 
lands of Sumatra, were to appear in open places on the mountains of Malaya. This 
species has larger fronds than M. forresiana, with reddish stipes and copious stiff 
spine-like scales throughout stipe and rachises. 


3. Pseudophegopteris Ching 1963: 313. Holttum 1969: 12 


Rhizome various, in the Malayan species erect, in P. aurita (Hook.) Ching 
long-creeping and slender. Stipe and rachis usually reddish, basal scales thin, 
red-brown when dry, edges not ciliate; scales on frond usually few, appressed, 
reduced to a single row of short cells with red transverse walls. Lamina usually 
large (smallest in the Malayan P. rectangulare), much longer than wide, with + 
reduced lower pinnae; in bipinnate fronds the lamina of pinnules adnate to 
pinna-rachis; hairs on frond acicular or short-capitate, always unicellular. Sori 
exindusiate, often spreading a little along the veins; sporangia sometimes bearing 
acicular hairs near annulus; spores pale, with a slightly raised reticulum of rather 
large meshes. 


Distribution: 21 species, distributed from the islands of St Helena and San 
Thomé (Atlantic Ocean) to Hawaii; in Malesia only on mountains in open places. 


The two Malayan species are named Thelypteris oppositipinna and T. brunnea 
in my book of 1955. Both names must be changed, and a new description of the 
latter is provided. The only other species which might occur in Malaya is P. aurita 
(Hook.) Ching, which was described from N.E. India and has been found on Mt 
Kinabalu and the highlands of eastern New Guinea; it might occur on the exposed 
upper parts of Gunong Tahan. In New Guinea this species was found to be tetrap- 
loid, but in Ceylon it is diploid. 


Pseudophegopteris rectangularis (Zoll.) Holttum 1969: 19. 
Basionym: Polypodium rectangulare Zoll., Syst. Verz. (1854) 37, 48. 
Name in Holttum 1955: Thelypteris oppositipinna (v.A.v.R.) Ching. 


Distribution: N.E. India; Sumatra, Malaya, Borneo, Java, at 3000-5000 ft. 


The name rectangularis was based on a specimen from Java, the later name 
Oppositipinna on a specimen from Sumatra; the species also received other names 
elsewhere (see Holttum 1969 for full synonymy). The few Malayan specimens have 
been found in rather dry exposed ground in or near stream-beds, whereas plants of 
P. paludosa (see below) grow in wet ground by streams. It would be interesting to 
transplant P. rectangularis to see whether different environmental conditions would 
cause it to vary from its normal characters as described and figured in my book. 


Pseudophegopteris paludosa (BI.) Ching 1963: 315. Holttum 1969: 23. 
Basionym: Polypodium paludosum Bl., Fl. Jav. Fil. (1851) 192, t. 90. 
Name in Holttum 1955: Thelypteris brunnea in part, excluding Indian plants. 


Correct name in Thelypteris: T. paludosa (Bl.) K. Iwats., Acta Phytotax. Geobot. 
19 (1961) 11. 


Rhizome erect, massive in well-grown plants. Stipe 50 cm or more long glab- 
rescent, reddish; basal scales to c. 10 x 2 mm, very thin. Lamina to 120 cm or 
more long; free pinnae to c. 15 pairs, opposite, lower pinnae somewhat reduced 
and more widely spaced, basal pinnae 25 cm long on a frond with largest pinnae 
33 cm; basal basiscopic pinnule or pinna-lobe longer than acroscopic. Pinnules 
broadly adnate to pinna-rachis, usually connected by a very narrow wing, grading 
distally to the deeply lobed apical part of the pinna; largest pinnules (apart from 
basal ones) about 4 x 1 cm, deeply lobed, veins pinnate in the lobes; lower surface 


150 Gardens’ Bulletin, Singapore —— XX1X (1976) 


of pinna-rachis and costae of pinnules bearing stiff spreading slender acicular hairs 
2-3 mm long, shorter and thicker hairs on upper surface. Sori usually 2 pairs in 


each pinnule-lobe, round or nearly so; sporangia lacking hairs near annulus. 


Distribution: Malesia, Sumatra to New Guinea, on mountains at 4000-7000 ft, 
in open wet ground by streams; rather few collections. 


When writing my bok of 1955 I had only seen one plant of this species, which 
I found in an early clearing (for the trout hatchery) near Brinchang at Cameron 
Highlands in the 1930’s; I also saw a plant collected by Mrs Allen at Fraser’s Hill. 
As Mrs Allen has reported (Gard. Bull. Sing. 17: 260. 1958) the species increased 
greatly in the later large clearings at the Highlands, and I saw it growing abundantly 
by streams above Brinchang village in 1969; these Malayan plants certainly agree 
closely with specimens from the mountains of West Java, whence Blume had the 
type of his species. 

The name Thelypteris brunnea applied to the Malayan species by me in 1955 
was based on Polypodium brunneum Wall., published without a description in a 
list of the specimens in Wallich’s herbarium. The earliest valid name for the Indian 
species is Phegopteris pyrrhorhachis Kunze, based on a specimen from the Nilgiri 
Hills in southern India; the rhizome is somewhat prostrate and the fronds are never 
so large as in P. paludosa. In Ceylon Prof. Manton found both tetraploid and hexa- 
ploid forms of this species. Malayan plants of P. paludosa look very uniform at 
Cameron Highlands. 


Mrs Allen remarked that she had found P. rectangularis and P. paludosa 
growing together, and it would not be surprising if intermediates were found. It 
should be noted that, apart from the great difference in size (which would not apply 
to young plants of P. paludosa) the two species differ constantly in the presence of 
stiff hairs on the sporangia P. rectangularis (see Holttum 1955 fig. 137) and their 
absence in P. paludosa. 

The plants from Mt Kinabalu mentioned by Mrs Allen in her note on Thelyp- 
teris brunnea above-mentioned are Pseudophegopteris aurita (Hook.) Ching. 


References to literature cited 


CHING, R. C. 1963. A re-classification of the family Thelypteridaceae from the 
mainland of Asia. Acta phytotax. sinica 8: 289-335. 


HOLTTUM, R. E. 1955. A Revised Flora of Malaya, 2, Ferns of Malaya. Govern- 
ment Printer, Singapore. 


1968. Ibid., second edition, with appendix of corrections and addi- 
tions. 


—_—_—— 1969. Studies in the family Thelypteridaceae, I. The genera Phegop- 
teris, Pseudophegopteris and Macrothelypteris. Blumea 17: 5-32. 


1971. Studies in the family Thelypteridaceae III. A new system of 
genera in the Old World. Blumea 19: 17-52. 


1976. Some new records of Thelypteridaceae for the Philippines. 
Kalikasan 5: 109-120. 


IWATSUKI, K. 1963-65. Taxonomy of the thelypteroid ferns, with special refer- 
ence to the species of Japan and adjacent regions, Parts 1-4, Mem. Coll, Sci. 
Kyoto Univ. B, 30: 21-51; 31: 1-40, 125-197. 


Tremellales with Tubular Hymenophores Found in Singapore 


by 
A. DAVID! & M. JAQUENOUD 
Laboratoire de Mycologie, associé au Achlenstr. 30, CH-9016 St Gall. 
CNRS, Villeurbanne, France Switzerland 
Summary 


The authors describe a new species of pore-bearing Tremellales: A porpium hexagonoides, 
and discuss a collection of a species closely related to A. dimidiatum David. 

Until recently, the poroid Tremellales were only represented by a resupinate 
species, Aporpium caryae (Scw.) Teix. & Rog. In a recent paper (David, 1974). 
a new species was described from Guadeloupe and named A. dimidiatum David. 
The author believed that the existence of Tremellales in the form of polypores 
might be far less exceptional than had been previously supposed. This opinion 
was confirmed by a short stay in Singapore? in July 1974 devoted to the study of 
the island’s polypores, when several poroid fungi with longitudinally divided 
hypobasidia were collected. On one hand the stay in Singapore was very profitable 
as far as the number of species collected was concerned, but on the other we were 
disappointed in the results of trying to culture them. From the spore samples 
made on the spot in Singapore, we should have got polyspermous and mono- 
spermous mycelium on our return to Lyon, but only a low percentage of germinating 
spores were found, probably due to the 7-15 days’ lapse before culturing. 
Are spores of equatorial species, developing in a climate which is always 
favourable for germination, particularly sensitive to drying out? The failure of the 
cultures, especially of monosperms, is to be regretted, because ome specimen 
collected in Singapore shows, apart from its size, many characteristic features of 
A. dimidiatum described from Guadeloupe: no microscopic difference could be 
discerned. On the other hand other specimens certainly represent a new species — 


Aporpium hexagonoides David & Jaquenoud, sp. nov. 


Fructificationes parvula*, solitaria, subdimidiata vel dimidiata, in statu recenti 
coriacea elastica; in statu sicco dura cornia, 2—3 cm lata, 1—1.8 cm ad radium, 
0.3-0.85 cm crassa. Facie superiore (Plate Ib) applanata vel leviter convexa, 
albida ad marginem, alibi pallide ochracea, 10 YR 8/6 7/6 7/8,4 molliter veluta 
(aut tomentosa) vel hispida in statu recenti; in arescendo corrugantur. Margine 
obtusa. Facie inferiore hymeniale (Plate la) pallide alutacea, 10 YR 8/2-2.5 
Y 8/2. Pori magni, angulosi, plus minusve hexagonales, ca. Imm diam. Multi 
fasces hyphacei ex hymenio eminentes, sub lente visibiles. Tubuli contexto 
concolori neque aparte separati. Systema hypharum dimiticum: hyphae sceleticae 


1Assisted by B. Dequatre, collaborateur Sexhtallaens du CNRS. 


2We are much indebted to the Chairman, Nature Reserves Board, Singapore and to Dr Chang 
Kiaw Lan for all the help given to us during our stay in Singapore. 


3We are very grateful to Dr. H. M Professor at the Cantonal G -School of 
iso gon’ tee voce etzger, anton rammar-School o 


4See “Code Munsell Book ps Onles” (1950), Baltimore. Maryland. 


151 


152 Gardens’ Bulletin, Singapore — XX1X (1976) 


hyalinae (3-) 4-5 » diam., crassis tunicatis usque ad 1 w hyphae generativae 
hyalinae tenuiter tunicatae, 2—3 » diam., cum articulis longissimis, ut fibulae 
rarae atque difficiles visu sunt (Fig. lb). Basidia claviformia 20 X 8 un, longi- 
tudinaliter septata in parte superiore (Fig. la), 4 sterigmatis subulatis, 10-12 
longis. Basidiospori hyalini, non cyanophili, non amyloidi, non dextrinoidi, sub- 
cylindreati, plus minusve depressi, cum regione apicali, Congo ammoniacali 
adhibito valde colorescente, 9-11 xX 4-5 y» (Fig. Ic). Inter basidia paraphysoidi 
subsunt simplices plus minusve ramosi. 


Haec species facile cognoscitur, quod pori magni saepe hexagonoides fiunt. 
Praeterea ab utraque alia specie nota magnitudine basidiorum atque spororum 
differt, et quod probasidium non prius quam in partibus superioribus dividitur. 


LY AD 1763 (holotypus in herbario A. David, Univ. Lugduni), ad truncum 
profunde in humo infossum, in margine silvae, Jungle Fall Valley Path, post 
casam, Bukit Timah Reserve, Singapore, 28.7.1974. 


Fruiting bodies small, solitary, subdimidiate to dimidiate, leathery and 
flexible when fresh, hard and horny when dried, 2—3 cm long, radius of 1—1.8 
cm, and 0.3 — 0.85 cm thick. Upper surface (Plate 1b) applanate to slightly convex, 
light ochraceous 10 YR 8/6 7/6 7/8 except towards the margin which is whitish, 
velutinous to hispid when fresh, becoming strongly radially wrinkled on drying. 
Hymenial surface pale brown between 10 YR 8/2 and 2.5 Y 8/2. Pores big 
angular, more or less hexagonal, about 1 mm. diam (Plate la). Numerous 
fascicles of hyphae emerging from the hymenium and visible under the hand-lens. 
Tubes and context concolorous and not distinctly separated. Hyphal system 
dimitic: skeletal hyphae hyaline (fig. 1b), 4-5 » diam., with walls up to 
1 » thick. Generative hyphae hyaline, with thin walls, about 2—3 yp», with very 
long cells, so that the clamp connections are rare and difficult to see. Basidia 
clavate, 20 X 8 », divided up longitudinally in the upper part (Fig. la), with 4 
sterigmata which are subulate and 10-12 y» long. Basidiospores hyaline, neither 
cyanophilous, nor amyloid, nor dextrinoid, with thin walls, subcylindric, more or 
less depressed, with one apical region which can be dyed strongly with ammoniacal 
Congo, 9-11 X 4-5 wu (Fig. Ic). 

This species is easily recognizable by its big pores which are often hexagonal. 
It differs from the other two known species of A porpium by the size of the basidia 
and of the spores, and by the fact that the probasidium is only divided up longi- 
tudinally in the upper part. 


Ecological and geographical distribution 


LY AD 1763 (holotype in the herbarium A. David, University of Lyon), on 
prostrate trunk, partly buried in the ground, at the edge of the forest, Jungle Fall 
Valley Path, behind the hut, Bukit Timah Reserve, Singapore. 28.7.1974. LY AD 
1820 on section of a trunk, within the edge of the forest, McRitchie Jungle, 
Singapore. July 1974. 


An Aporpium sp. very similar to A. dimidiatum 


This species, which we collected only once in Singapore presents so many 
similarities with Aporpium dimidiatum that we prefer to be cautious and not to 
make it a new species, at least for the time being. It differs from A. dimidiatum in — 
the small size of its fruiting bodies, the smaller pores, and in being constantly — 
sulcate. Fruiting bodies, many, small, dimidiate to effused-reflexed, solitary or more 
or less confluent in longitudinal stripes, 2.5-3 cm long, radius 1.5 cm, 0.7-8.0 cm — 
thick, becoming very hard after drying. Upper surface convex, not hairy, but — 
showing a fine tomentum under the hand-lens, beige to light rust 10 YR 8/3 7/3 
7/4. Marginal area usually with 2-3 concentric grooves, the rest of the upper 
surface more or less scrobiculate. Context leathery, strongly zoned with brown 


Plate 1. Fruitbody of Aporpium hexagonoides (x3) 
a: hymenial surface, b: upper surface. 


Tremellales 153 


stripes of cartilaginous consistency corresponding to growing layers. Hymenial 
surface greyish white, becoming brown when touched: (5—) 8-10 pores per mm. 
Microscopic characters: all identical to those of A. dimidiatum. 


BAO 
3 a 


Fig. 1. a: fragment of the hymenium squashed after one night in ammoniacal Congo (x 2000) 
b: skeletal and generative hyphae (x 2000). 
c: spores (x 3000). 


Reference 


DAVID, A. 1974. Aporpium dimidiatum, nouvelle tremellale porée. Bull. trimest. 
Soc. mycol. Fr. 90: 179-185. 


ea rani Muti FIC] ticlisabondn 
ete: 28 
= i ae EF Pat 


Sur Un Nouveau Bolet Tropical 4 Spores Ornées 


par 


JACQUELINE PERREAU et RocER HEIM 


Laboratoire de Cryptogamie, Muséum National d'Histoire Naturelle, Paris 


Résumé 


Originaire du Gabon, ie Boletus cornalinus est un Xerocomus entiérement moucheté du 
méme rose-pourpre que celui qui teinte les pores, tandis que la chair et les tubes se révélent 
incarnats; il posséde des spores brun jaunatre 4 ornementation peu accentuée, d’irréguliérement 
et densément fovéolée 4 verrucoso-cristulée. I] s’apparente 4 d’autres bolets appartenant aux 
sous-genres Phylloporus et Xerocomus dont certaines espéces montrent des spores non lisses; 
ses affinités plus lointaines pourraient se trouver du cété des Piperati. 


Summary 


Boletus cornalinus, originating from Gabon, is a Xerocomus entirely spotted with the 
same purple rose colour that characterizes its pores, with the flesh and tubes being incarnate. 
Spores yellowish brown, finely ornamented; ornamentation irregularly and densely foveolated 
to verrucose-cristulate. Related to other Boletes, especially of subgenera Phylloporus and 
Xerocomus where some species exhibit non-smooth spores. Its remote affinities could be 
traced to the Piperati group. 


A laube du XXéme siécle, on ne connaissait guére qu’une quinzaine de bolets 
a spores ornées avec, parmi eux, le cosmopolite Boletus strobilaceus Scop. ex. Fr. 
sur lequel Berkeley créa, dés 1851, le genre Strobilomyces et le Boletus ananas 
Curtis qui devint le type du genre Boletellus établi, en 1909, par Murrill. Actuelle- 
ment, il est possible d’en compter plus de soixante-dix, découverts notamment au 
fur et 4 mesure que se développait l’étude des flores tropicales: ils se trouvent 
répartis dans plusieurs coupures génériques ou sous-génériques selon les con- 
ceptions des Auteurs sur la systématique des Bolétales. Bien qu’ayant la 
caractéristique commune de présenter une ornementation sporale, ces espéces se 
rattachent 4 des groupes différents au sein de ]’ensemble formé par les champignons 
charnus 4 hyménophore tubulé et, si les indications tirées de leurs spores ne 
peuvent étre seules décisives pour leur classement, du moins suggérent — elles 
souvent des regroupements, affinités ou tendances; ainsi en est-il pour la forme de 
ces éléments, leur pigmentation et les particularités architecturales de leur paroi 
qui se manifestent essentiellement au niveau de l’exospore. 


Tous ces bolets montrent justement une assez grande diversité dans les 
motifs de décoration exosporique : 4 cété de réseaux serrés et profonds, d’une 
ordonnance presque réguliére, ou d’épaisses nervures longitudinales, on observe des 
verrues plus ou moins massives, des crétes, des ailes élevées ou de fines stries, 
des nappes fovéolaires d’une extraordinaire variabilité, des réseaux contournés, 
incomplets ou formés d’amples alvéoles. Evidemment, selon les espéces, l’orne- 
mentation ne présente pas la méme importance et apparait parfois si faible 
qu’on la distingue 4 peine au microscope photonique et qu'il faut étudier ses 
détails en microscopie électronique a balayage. 


_ Tel est le cas chez un bolet recueilli, 4 plusieurs reprises, par M. Gérard 
Gilles, dans la forét de la Mondah, prés de Libreville, au Gabon, forét qui abrite 
une flore fongique particuliérement riche et intéressante, peu connue encore. 
Entiérement rose pourpré a incarnat, comme I’est la variété de calcédoine appelée 
cornaline, cette espéce nouvelle a recu le nom de Boletus (Xerocomus) cornalinus. 


155 


156 Gardens’ Bulletin, Singapore — X XIX (1976) 


20 ym 

Cc 
Fig. 1. Boletus cornalinus: a — Carpophore et coupe dans le chapeau; b — spores, dont | 
pleurocystides; d — | 


une en coupe optique, vues au microscope photonique; c — 
hyphes du revétement piléique., 


Un Bolet Tropical 157 


Description 
Caractéres macroscopiques 


Chapeau de 20-60 mm de diamétre et jusqu’ a 20 mm d’épaisseur, convexe, 
puis convexe-aplani, régulier, sec, entiérement moucheté de flocons rose pourpré, 
vieux rose, rose vineux (Séguy 82 et 83)* sur un fond plus clair, rosé (S 80), 
Yensemble passant lors de la dessiccation 4 un brunatre mélé de tons rouillés- 
cuivrés; marge arrondie, trés légérement excédante, parfois de teinte plus pale; 
revétement non séparable. 


Chair de 5 4 10 mm d’épaisseur, séche, d’un blanc-rose pourpré, incarnat, 
proche de S 130, jaunissant a l’air en deux a trois minutes. 


Hyménophore tubulé, horizontal ou faiblement ventru, échancré autour du 
sommet du pied selon des lamelles décurrentes en filet sur celui-ci; tubes longs 
de 5-15 mm, blanc rosé (S 130), immuables, mais devenant brun-jaune lorsqu’ils 
sont poudrés par la multitude des spores, 4 pores arrondis au début, puis suban- 
guleux, assez réguliers, de 0,6-1 mm de diamétre, rose vineux (S 82), nettement 
plus vermillon (S 93-94) sur exsiccata. 


Pied relativement gréle, de 50-100 mm de longueur, atteignant 6-8 mm de 
diamétre et 10 mm 4 la base vers laquelle il se dilate progressivement, fibreux, 
plein, entiérement couvert de flocons et de courtes fibrilles rose pourpré (S 82); la 
base est plus ou moins enveloppée d’un manchon de mycélium beige rosé d’ot 
partent quelques rhizomorphes brun noiratre assez gros et tenaces (Fig. 1, a). 


Couleur des spores en masse : brun jaune. 
Odeur inconnue. 
Saveur légérement acidulée. 


Caractéres macrochimiques 


NH,OH : instantanément jaune-brun verdatre sur le revétement et la chair — 
Acides : réaction nulle — FeSO, : immédiatement brunatre sur la chair piléique 
— lode (Réactif de Melzer) : réaction nulle sur la chair. 


Caractéres microscopiques 


Basides sub-ellipsoides, de 25-30 X 10-12 um, portant quatre stérigmates 
effilés, peu arqués, longs de 5 »m en moyenne. 


Spores de (13) — 13,5 — 15 X 4,5 — 5,5 — (6,2) um, ellipsoides-fusiformes, 
longuement atténuées vers le sommet arrondi, subtilement aplati parfois; avec, a 
maturité, une dépression supra-appendiculaire accentuée, la face dorsale offrant 
souvent une convexité, puis une légére concavité juste au-dessus de l’appendice 
hilaire petit et subcylindrique; 4 gouttelettes lipidiques assez nombreuses; 4 paroi 
ornée, jaune brunatre; non amyloides. 


Au microscope photonique (Fig. 1, b), l’ornementation, peu accentuée, apparait 
composée de multiples ponctuations délicates et de taches un peu arrondies ou 
étoilées-divariquées, parfois disposées en alignements, brunatres ou jaune 
réfringent selon la mise au point. En coupe optique, cette ornementation se traduit 
par des échancrures festonnées dans une exospore colorée, alors qu’épispore et 
endospore sousjacentes demeurent d’épaisseur réguliére. Toutefois, certaines spores 
montrent des plages pratiquement lisses. 


Naturellement, les observations en microscopie 4 balayage précisent les détails 
d'un relief qui, dans ces conditions, se révéle moins masqué par la périspore et 
Yectospore. En voyant les nombreuses fossettes ou anfractuosités plus ou moins 
fusionnées, isolant de petites crétes contournées et irrégulitrement anastomosées ou 
des protubérances versiformes (PI. I, A-D), on ne peut que penser aussitét a 
une nappe fovéolaire. Toutes les caractéristiques de ce type ornemental sont 


*— BE, Séguy — Code universel des couleurs. P. Lechevalier, Paris, 1936. 


158 Gardens’ Bulletin, Singapore — XX1X (1976) 


d’ailleurs réunies puisque l’on retrouve des plages de surface sporale lisses, 
surtout au sommet, ou a peine scrobiculées comme sur la zone entourant l’appendice 
hilaire (en B); a l’opposé, l’aspect déchiqueté et “‘cunéiforme”’ de la décoration se 
remarque sur toutes les photographies de la planche. 


Pleurocystides fusiformes 4 sommet étiré-atténué, parfois capité, toujours 
émoussé (Fig. 1, c), de 50-65 xX 12-15 wm, 45 pm au col, a paroi fine, a 
contenu jaune brunatre, légérement flexueuses, émergentes, relativement abondantes 
(547 par 100 pm?). 


Cheilocystides peu différenciées sur l’aréte des tubes, larges de 7-15 pm, 
tres nombreuses et couvertes de granulations polygonales-arrondies, de 0,2-0,5 
um de diamétre, rouge orangé vif trés réfringent. 


Trame des tubes de type Phylloporus et Xerocomus; hyphes hyalines, larges 
de 5-7 pm, non bouclées, 4 peine divergentes. 


Revétement piléique constitué d’hyphes entrecroisées, incrustées, de largeur 
variable (5-16 »m), étranglées aux cloisons et dont les articles terminaux, longs de 
30-35 ym, sont cylindracés ou clavulés. 


Ces hyphes que |’on voit également en bouquets dans les flocons du pied, sont 
recouvertes de granulations semblables a celles observées sur les poils de l’aréte 
des tubes. Dans les préparations montées avec NH,OH, elles se révélent seulement 
hyalines-réfringentes, car leur teinte rouge orangé vif disparait sous l’action de ce 
produit (Fig. 1, d). 


Habitat et répartition géographique 

A terre, parmi les feuilles, en forét ombrophile. Forét de la Mondah, km 31:5, 
environs de Libreville, Gabon. Leg. Gérard Gilles, 13-10 et 10-11-1968, n° Div. 
Gab. 33 (type) — Autres récoltes : 20-10-1968, n° Div. Gab. 39 et 21-09-1969, 
n° Div. Gab. 33. 


Boletus (Xerocomus) cornalinus Perreau et Heim, sp. nov. 


Pileus 20-60 mm latus, usque 20 mm crassus, convexus ad applanatum, 
omnino e purpureo-roseo ac vinoso floccosus, interstitiis dilute roseis. Caro incar- 
nata, mox in aere flavescens, sapore acidulo. Tubi incarnati, postice breviores, 
semoti, lamellis decurrentes circum stipitis apicem; pori purpureo-rosei, suban- | 
gulares. Stipes comparate gracilis, 5|0 — 100 mm longus, 6 — 8 mm diametro, basi — 
leviter dilatatus, pileo concolor, mycelio isabellino, rhizomorphis umbrinis. Sporae 
(13) - 135-15 xX 4.5 — 5.5 — (6,2) yp, ellipsoideo-fusiformes, brunneolo-flavae, — 
haud amyloideae, minutissime punctulatae, per microscopium electronicum ex — 
irregulariter denseque foveolatis verrucoso-cristatae. Pleurocystidia numerosa, — 
50 - 65 X 12 — 15 yp, elongato apice fusiformia, projicientia, brunneo-flavo succo | 
impleta; cheilocystidia multis cinnabarinis NH,OH decolorantibus granulis incrus- 
tata; hyphae cuticulares pilei stipitisque similiter tectae. Hyphae afibulatae. Ad 
terram in silva — Libreville, Gabon — leg. G. Gilles, 13-10 ac 10-11-1968, n° 
Div. Gab, 33 (typus PC). 


La mise en évidence d’une ornementation sporale chez ce bolet africain aurait 
pu conduire a le placer dans le genre Boletellus; il ressemble en effet quelque | 
peu aux B. obscurecoccineus (Hohn.) Singer et B. cardinalicius Heim et Perreau | 
dont cependant les longues spores sont finement striées; par d’autres caractéres, il | 
paraitrait se rapprocher du B. purpurascens Heinem. Or, tout récemment, E. J, H. 
Corner a suggéré que cette derniére espéce, 4 spores largement elliptiques et 
fortement verruqueuses, pourrait appartenir, ainsi que le B. shichianus (Teng et | 
Ling) Teng a spores verruculeuses, au sous-genre Punctispora_ qu il a établi avec. 
comme représentants, les B. betula Schw. et B. punctisporus Corner, Ces champi- | 
gnons possédent précisément de grandes spores couvertes d’une nappe fov | 


Un Bolet Tropical 159 


qui déploie toute la variabilité de détail qu’une telle décoration implique — toutefois, 
il s’agit simplement d’un phénoméne de convergence, car le B. cornalinus s’éloigne 
d’eux par d’importantes différences liées a la réticulation du pied, la teinte jaune, 
puis olivacée de ’hyménophore, le bleuissement de la chair, etc... 


Ces deux derniéres caractéristiques se révélent également propres 4 de 
nombreux Xerocomus dont s’écarte aussi notre espéce gui n’est pas sans évoquer 
cependant le B. versicolor Rostk. des régions tempérées; elle pourrait étre, de plus 
prés encore, comparée aux B. puniceus Chiu et B. roseolus Chiu, du Yunnan, aux 
B. phoeniculus Corner et B. albipurpureus Corner, de Malaisie. Avec ses hyphes 
incrustées, le B. cornalinus toucherait au groupe du B. chrysenteron St—Amans 
et se rapprocherait légérement de certains représentants tropicaux de cet ensemble, 
décrits notamment par E. J. H. Corner (B. catervatus, B. satisfactus) et qui offrent 
une chair jaunatre ou blanche, immuable. L’existence d’incrustations sur les hyphes 
cuticulaires se montre d’ailleurs fréquente chez les bolets et M. Josserand a déja 
noté pour le B. porphyrosporus [Porphyrellus porphyrosporus (Fr. et Hok) Gilb.], 
l’action dissolvante de l’ammoniaque sur le pigment “‘avec persistance de la masse 


TOR 


primitivement pigmentée”’. 


D’un autre cdété, on peut noter certaines ressemblances entre le bolet gabonais et 
les Xerocomus 4 pores rouges de Nouvelle-Zélande [X. macrobbii McNabb peut- 
étre, X. nothofagi McNabb et surtout X. rufostipitatus McNabb a chair créme] ou 
de Malaisie [B. rubriporus Corner, toutefois 4 chair bleuissante]. Enfin, et de méme 
que pour ceux-ci, on peut penser, (car le B. cornalinus rappelle le B. amarellus 
Quélet), 4 des relations lointaines avec le groupe des Piperati, plus particuliérement 
avec des espéces nord-américaines telles que Boletus pseudorubinellus Smith et 
Thiers, B. rubritubifera Kauffman, B. rubinellus Peck; il faut remarquer pourtant que 
les réactions colorées obtenues sous l’influence de NH,OH ou de FeSO, ne 
concordent pas. 


L’insertion d’une espéce a spores ornées dans le sous-genre Xerocomus ne peut 
guére surprendre puisque de nombreux Boletellus, dont les éléments sporaux 
apparaissent trés finement costulés, se situent au voisinage immédiat de ce 
taxon et peut-étre méme en dépendent. D’autre part, si E. J. H. Corner men- 
tionne l’éxistence probable d’une légére striation chez le B. (Xerocomus) albipur- 
pureus, Yun de nous (J.P. 1965) signalait la présence de lignes, d’ondula- 
tions exosporiques chez le B. subtomentosus Fr. Grace a des observations 
au microscope électronique a balayage, Moore et Grand 1970, ont montré, 
que les basidiospores du Phylloporus rhodoxanthus (Schw.) Bres. n’étaient pas 
lisses; leur surface porte, en effet, une multitude de protubérances fusiformes, 
enchevétrées, souvent caténulées ou paralléles entre elles. De notre cdté et avec 
cette méme technique (J.P., inédit), des recherches ont permis d’examiner de 
facon plus précise le relief entrevu sur les spores de nombreux exemplaires de 
B. subtomentosus, mais aussi de le déceler chez le B. parasiticus Fr. : extrémement 
peu accusé, il se manifeste en général par de délicates nervures ou par des saillies 
allongées, disposées en tous sens. Sur certaines spores, des fossettes, ainsi que des 
anfractuosités irréguliéres sont visibles. L’agencement désordonné de _ petites 
crétes en fuseau et a profil arrondi constitue un motif de décoration qui se révéle 
bien différent des nappes fovéolaires que l’on trouve chez le B. cornalinus; 
il ressemble fort, par contre, a celui observé sur les spores d’un champignon tout 
autre, Hericium coralloides (Scop. ex Fr.) S. F. Gray, chez qui la taille des 
protubérances est cependant plus grande. 


Divers aspects d’architecture exosporique sont donc présents chez les 
Xerocomus; il est vraisemblable que d’autres seront décelés, reflétant et accentuant 
encore l’hétérogénéitré de ce vaste sous-genre de bolets, mais sans doute 
Yexamen de ces aspects aidera-t-il 4 la recherche d’une interprétation systématique 
plus naturelle de ce groupe. 


160 Gardens’ Bulletin, Singapore — XXIX (1976) 
Notes Bibliographiques 


CHIU, W. F. 1948. The boletes of Yunnan. Mycologia 40: 199-231. 


CORNER, E. J. H. 1970. Phylloporus Quél. and Paxillus Fr. in Malaya and 
Borneo. Nova Hedwigia 20: 793-832, 8 fig., 8 pl. 

1972. Boletus in Malaysia. Bot. Gardens, Govern. Print. Off., 
Singapore, 263 pp., 80 fig., 23 pl. 

1974. Boletus and Phylloporus in Malaysia: further notes and 
descriptions. Gdns’ Bull. Singapore 27: 1-16, 1 fig. 

HEIM, R. & J. PERREAU 1963. Le genre Boletellus 4 Madagascar et en Nou- 
velle-Calédonie. Revue Mycol. 28: 191-199, 6 fig., 1 pl. 

HEINEMANN, P. 1954. Flore Iconographique des Champignons du Congo, 
Bruxelles. 3¢me fasc.: Boletineae: 49-80, 3 pl. 

JOSSERAND, M. 1952. La description des Champignons Supérieurs. P. Leche- 
valier, Paris, 338 pp. | 
McNABB, R. F. R. 1967. The Strobilomycetaceae of New Zealand. N.Z. Jl Bot. 

5: 532-547, 3 fig. 
1968. The Boletaceae of New Zealand. N.Z. JI Bot. 6: 137-176, 
8 fig. 

MOORE, R. T. & L. F. GRAND. 1970, Application of scanning electron micro- 
scopy to basidiomycete taxonomy. Proceedings IlIrd Ann. Scann, Electr. 
Microsc. Symp., Chicago, 7 pp., 33 fig. 

PERREAU-BERTRAND, J. 1961. Recherches sur les ornementations sporales et 
la sporogenése chez quelques espéces des genres Boletellus et Strobilomyces 
(Basidiomycetes). Annls Sci. nat., Bot., 12eme série, 2: 399-489, 35 pl. 

1964. Complément a l’étude des ornementations sporales dans le 
genre Boletellus. Annls Sci. nat., Bot., 12@me série, 5: 753-766, 5 pl. 

1965. Structure membranaire et différenciations apicales chez les 
spores des genres “‘Xerocomus, Boletellus, Heimiella et Strobilomyces’’. 
C. r. hebd. Séanc. Acad. Sci., Paris 260: 4245-4248, 1 fig. 

1974. Variations sur un theme ornemental : le réseau des basidio- 
spores, Trav. myc. dédiés a R. Kiihner, Numéro spécial, Bull, Soc. Linn. Lyon 
43: 327-338, 1 fig., 2 pl. st 

PERREAU, J. & R. HEIM. 1969. L’ornementation des basidiospores au microscope 
électronique a balayage. Revue Mycol. 33 (1968): 329-340, 3 fig. 4 pl. 

SINGER, R. 1945. The Boletineae of Florida with notes on extralimital species, I. 
The Strobilomycetaceae. Farlowia 2: 97-141, 1 pl; II. The Boletaceae 
(Gyroporoideae). Ibid. 223-303, 1 pl. 

—_—_—_———— 1962. Agaricales in Modern Taxonomy. 2nd ed. J. Cramer, Wein- 
heim, 915 pp., 73 pl. 

1964. Boletes and related groups in South America, Nova Hedwigia 
7: 93-132, 4 pl. 

SMITH, A. H. & H. D. THIERS. 1971. The Boletes of Michigan. The University 
of Michigan Press, Ann Arbor, 428 pp., 133 fig., 157 pl. 

SNELL, W. H. & E. A. DICK. 1970. The Boleti of Northeastern North America. 
J. Cramer, Lehre, 115 pp., 87 pl. 

TENG, S. C. 1964. Champignons de Chine. Pékin, 808 pp. 

WATLING, R. 1970. Boletaceae-Gomphidiaceae-Paxillaceae. British Fungus 
Flora Ag. and Boleti. Royal Botanic Garden, Edinburgh, 125 pp., 108 fig. 


Planche I. Spores du Boletus cornalinus vues au microscope électronique a balayage. 
(Cl. Lab. Géol. Muséum, Paris) 


A — Divers aspects de l’ornementation fovéolée et verrucoso-cristulée; 

B — Spore en profil frontal, montrant une zone nettement fovéolée autour de l’appendice 
hilaire; 

C —Spore en profil dorsi-ventral, 4 ornementation trés déchiquetée, verruqueuse et 
cristulée; 

D — Détail de lornementation en nappe fovéolaire trés densément creusée. 


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Development of Primary Secretary Ducts in the Stem of 
Mangifera indica L. (Anacardiaceae) 


by 
A. FAHN and D. M. JOEL 


Department of Botany, The Hebrew University of Jerusalem, Israel 


Summary 


The development of primary secretory ducts of stems of Mangifera indica L. has been 
studied with the aid of the electron microscope. The duct cavity has been found to be formed 
lysigenously. The primary ducts start to develop in the young leaf primordia. There the 
future epithelial cells still contain very large central vacuoles. These cells envelope a single 
file of cells which disintegrate and initiate the duct cavity. In the stem the duct cavity 
enlarges by lysis of epithelial cells and neighbouring cells become epithelial. In open ducts 
wall-remains of disintegrated cells are found attached to the active epithelial cells. 


Introduction 


Many early botanists with their excellent minds and with the aid of the then 
available equipment presented descriptions of the structure of cells and tissues, 
which, when examined many years later with the aid of the electron microscope, 
were usually found to be accurate. However, new embedding and sectioning 
techniques for light microscopy and the use of the electron microscope for anatomi- 
cal investigations have in many cases added important new information to the 
understanding of developmental processes of cells and tissues. 


The mode of initiation and development of cavities of internal secretory 
structures of plants has been dealt with mainly in early studies. Various investiga- 
tors often held contradictory views as to whether cavities of specific ducts develop 
schizogenously, lysigenously or schizo-lysigenously (cf. Carr and Carr, 1970). 


The ducts of the Anacardiaceae were examined by many researchers. The 
views on the manner of formation of the duct cavity in the different species and 
organs vary to a great extent (Miiller, 1866-67; Sieck, 1895; Tschirch, 1900; 
Venning, 1948; Varghese and Pundir, 1964; Fahn and Evert, 1974). While 
studying the ducts of Mangifera indica and the way their cells produce and 
eliminate their secretory substance, we also tried to clarify the manner of duct 
cavity development in the different plant organs, with the aid of the electron 
microscope. 


The present paper deals with the development of the primary shoot ducts. 


Material and Methods 


Stem portions from the apical region and from mature internodes of one-year- 
old saplings of mango (Mangifera indica L.) were used for examination. The 
saplings were grown in a greenhouse at the Hebrew University of Jerusalem. 


For light microscopy hand cut sections were used. 


For electron microscopy small portions of tissues including ducts were fixed 
in 6% glutaraldehyde for 2 hours, postfixed in OsO, 2% for 2 hours (both in 
cacodylate buffer O.1M pH 7.2), dehydrated in ethanol and embedded in Spurr’s 
low viscosity embedding medium (Spurr, 1969). Sections were cut on LKB 


161 


162 Gardens’ Bulletin, Singapore — X XIX (1976) 


ultrotome III, stained with uranyl acetate and lead citrate, and examined with a 
Philips 300 electron microscope. 


Observations 


In the stems of mango (Mangifera indica) the primary secretory ducts occur 
in the phloem and pith (Plate 1, A-C). The mature duct consists, in cross section, 
of a cavity which is surrounded by a few concentric rows of cells which are more 
or less isodiametric or somewhat flattened and smaller than those of the neighbour- 
ing tissues. In the direction of the long axis of the duct they are elongated. No 
distinct intercellular spaces occur between these cells. The cells of the row 
neighbouring the cavity do not differ much from the cells of the other rows. They 
contain a large central vacuole and a thin layer of cytoplasm (Plate 2, A). In the 
duct cavity the secreted material is confined to its periphery. Most of the secreted 
material is exuded from the duct cavity during cutting of the stem and the fixation 
of the material. 


The ducts start to differentiate in the shoot apex. In order to follow their 
development, successive sections, starting about 6 mm from the shoot tip and 
proceeding upwards, were examined. In the upper young region of the stem most 
of the cells neighbouring the duct cavity, the epithelial cells, are rich in cytoplasm 
and contain only a few very small vacuoles (Plate 2, B; Plate 4, A). The 
cytoplasm of these cells is dense, the ER is well developed. Parallel aligned ER 
elements have sometimes been seen to occupy a large part of the cytoplasm 
(Plate 4, A). The nuclei are relatively large. Plastids and mitochondria are 
numerous, Golgi bodies are occasionally observed in groups (Plate 3, A). 
Osmiophilic droplets are common and often in association with plastids and Golgi 
bodies (Plate 3, A; Plate 4, A, B). The process of secretion and sites of synthesis 
of the secretory substances in the cells will be treated in a separate article. 


The duct cavity in the young portions of the stem is filled with electron dense 
secreted substances (Plate 4, B). 


At the level of about 6 mm from the tip of the shoot apex single cells with 
a large vacuole and a very thin layer of cytoplasm are observed among the typical 
epithelial cells. Cell ‘‘a” in Plate 2, B gives the impression of joining the row of 
the densely stained epithelial cells after having divided from a cell situated behind 
them. In the gap where this cell is seen to join the epithelial cells, remnants of 
the back wall of an epithelial cell which has apparently undergone lysis can be 
seen. The region of the middle lamella between the wall of the joining cell and the 
remains of the wall of the disintegrated epithelial cell can clearly be observed. 


In a section at a somewhat higher level (Plate 4, A), two small, narrow and 
deformed epithelial cells (d) with a dark disordered content are present. Between 
two unchanged epithelial cells a wide gap (g) can be seen in the same section. 
Part of the gap is occupied by electron dense material. One may assume that a cell 
which was in this place has disintegrated. Wall remains of the missing cell are 
seen attached to the neighbouring cell of the row surrounding the epithelial cells. 
In addition to outer cells joining the epithelial cells new cells are formed by 
anticlinal division of the epithelial ones. Between the cytoplasm of the epithelial 
cells and their walls, mostly in the region facing the duct cavity, large spaces occur 
containing vesicular and membranous structures, as well as very dark osmiophilic 
material (Plate 4, B). A thin layer of osmiophilic material often surrounds the — 
entire cytoplasm. 


In all sections, walls of the epithelial cells facing the cavity consist of two 
layers between which a distinct middle lamella can be seen. The middle lamella 
is swollen in many places (Plate 3, A, B). The layer closer to the cavity is 
irregularly fringed. This layer apparently represents remains of walls of the cells 
which have disintegrated. 


Mangifera indica, secretory ducts 163 


The continuation of the stem ducts was followed in the leaf primordia 
situated less than 1 mm from the tip of the shoot apex. In the stem, before 
entering the primordia, the epithelial cells which are rich in cytoplasm were seen, 
in cross section, to surround a cell with a disintegrated protoplast (Plate 5A). In 
the leaf primordium itself the future epithelial cells contained large central 
vacuoles and thin layers of cytoplasm. As at the base of the leaf, at the site of the 
future duct cavity a single cell with a disintegrated protoplast was found in cross 
sections, at least up to one third of the height of the leaf primordium (Plate 5, B). 
In few places initial stages of disintegration were also observed in the cell wall. 


Discussion 


Diverse views of the mode of development of the duct cavity in the Anacar- 
diaceae have been held by different authors. Engler (1896) dealing with the 
family, McNair (1918) who investigated Rhus diversiloba Torr. and Gray, and 
Fahn and Evert (1974) who investigated the secondary phloem ducts of Rhus 
glabra Thunb. stated that the ducts develop schizogenously. Sieck (1895), who 
worked on stems and fruits of Anacardium occidentale L. reported that the ducts 
originate schizogenously, but that continued development is lysigenous. Such a 
mode of duct development in Anacardiaceae was also reported by Tschirch 
(1900). Venning (1948) came to the conclusion that the manner of development 
of duct cavities varies among plant organs being of schizogenous origin in stems 
and leaves of Schinus and fruits of mango of schizo-lysigenous origin in stems and 
leaves of Spondias and mango and of lysigenous origin in floral organs (with the 
exception of the ovary) in mango. Varghese and Pundir (1964) reported that in 
the pseudocarp of Anacardium occidentale the ducts develop lysigenously. 


The present electron microscopical investigation on the primary secretory 
ducts of the stem of mango showed that the cavities of these ducts initiate and 
develop lysigenously. The stem ducts initiate in the leaf primordia situated very 
close to the tip of the shoot apex. In the centre of the developing duct there is a 
single file of cells. The cells of this file disintegrate, initiating the development of 
the duct cavity. 


In the stem, the duct cavity enlarges by lysis of epithelial cells, and neighbour- 
ing cells become epithelial. A proof for lysis of cells may be found in that remains 
of additional cell walls can be seen on the surface of the epithelial cell 
walls facing the duct cavity. Between these remains and the intact epithelial cell 
walls a middle lamella with occasional swellings can clearly be observed. It can 
thus be concluded that the lysis of the wall starts from inside the cell and progresses 
towards the middle lamella. This differs completely from the manner of wall lysis 
during schizogenous development of intercellular spaces of duct cavities (Fahn 
and Benajoun, in preparation). 


Fractures occurring in the separation zone of leaves were also reported to be 
a result of the dissolution of the middle lamellar region of cell walls (Sexton and 
Hall, 1974). 


The succession of wall lysis as seen in the mango ducts differs also from that 
reported by Tschirch (1889) for gum duct formation. There, according to Tschirch, 
the disintegration of walls starts in the primary walls and then proceeds in the 
secondary wall. The wall lysis in the cells of mango stem ducts differs therefore 
basically in mode of succession from that occurring in schizogenous processes and 
lysigenous formation of gum ducts. 


Concurrently with the further process of cell lysis radial (anticlinal) divisions 
of epithelial cells may apparently take place. However, the initial stage of duct 
formation is strictly lysigenous. 


164 Gardens’ Bulletin, Singapore — XX1X (1976) 


Acknowledgement 


The authors wish to thank The Department of Horticulture of the Volcani 
Institute at Bet Dagan for kindly supplying the seeds from which the mango 
saplings were grown, 


References 
CARR, D. J. & S. G. M. CARR, 1970. Oil glands and ducts in Eucalyptus 


V’Hérit. II, Development and structure of oil glands in the embryo. Aust. J. Bot. 
18: 191-212. 


ENGLER, A. 1896. Anacardiaceae. In: A. Engler and K. Prantl (ed.), Die 
natiirlichen Pflanzenfamilien III, 5. 


FAHN, A. & R. F. EVERT, 1974. Ultrastructure of the secretory ducts of Rhus 
glabra L., Am. J. Bot. 61: 1-14. 


McNAIJIR, J. B. 1918. Secretory canals of Rhus diversiloba, Bot. Gaz. 65: 268-273. 


MULLER, N. J. C. 1866-67. Untersuchungen tiber die Vertheilung der Harze, 
atherischen Oele, Gummi und Gummiharze, und die Stellung der Sekretions- 
behalter im Pflanzenk6rper. Jb. wiss. Bot. 5: 387-421. 


SEXTON, R. & J. L. HALL, 1974. Fine structure and cytochemistry of the 
abscission zone cells of Phaseolus leaves. I. Ultrastructural changes occurring 
during abscission. Ann. Bot. 38: 849-854. 


SIECK, W. 1895. Die Schizolysigenen Sekretbehalter. Jb. wiss. Bot. 27: 197-242. 


SPURR, A. R. 1969. A low-viscosity epoxy resin embedding medium for electron 
microscopy. J. Ultrastruct. Res. 26: 31-43. 


TSCHIRCH, A. 1889. Angewandte Pflanzenanatomie, Band I. Urban & Schwar- 
zenberg, Vienna. 


1900. Die Harze u.d. Harzbehalter. Gebriider Borntraeger, Leipzig. 


VARGHESE, T. M. & Y. P. S. PUNDIR, 1964, Anatomy of the pseudocarp in 
Anacardium occidentale L., Proc. Indian Acad. Sci. 59: 252-258. 


VENNING, F. D. 1948. The ontogeny of the laticiferous canals in the Anacar- 
diaceae. Am. J. Bot. 35: 637-644. 


Facing Page 


Plate 1. Micrographs of hand cut cross-sections of a stem, showing A, primary (phd) 
and secondary (sd) phloem ducts, x 120; B, one primary phloem duct, x 300; C, a pith duct 
(pd), x 300. 


Plate 2. Electron micrographs of cross- 


sections of primary 


c — duct cavity, wr — wall remnant of disintegrating cel n du 
showing a gap (g) in the epithelium apparently formed by disintegration of an epithelial 


cell. A neighbouring outer cell (a) is seen 


to join the gap, * 


ducts. A, mature phloem duct; 
1, X 5000; B, young pith duct 


4600. 


Plate 3. 
around the duct cavity, wall 
Wr — wall remains. A, X 40,000; B, x 30,000. 


Electron micrographs of cross-sections of portion of young pith ducts showing, 


Temains of disintegrated cells. ml — middle lamella. 


Plate 4. As 
xX 4000; B, 
with vesicula 


See oS 


in plate 3. A, showing 2 


showing i 


n epithelial cel 


SSN 
x 
RAY WAN x 
Y . 


deformed cells (d) and a gap (g) in the epithelium, 


Is spaces (s), between pro 


r and lamellar structures, x 3700. 


toplast an 


d walls, filled 


Plate 5. A, Electron micro 


of a leaf primordium. X 5000; 


B, A cross-section of the duct shown in A but in the leaf primordium. 
X 5000. 


graph of a cross-section of a pith duct close to the base 


: ; ‘ Aer gs 
Se Rs Oi et st iy ee | rg a 
ett? orrite . 
ar . “4 ove Wy! Dries 4 tN + 
Wide cane 4 3} we a oy. 7 
war . ‘ <9 


Girdling Vascular Bundles in Dicotyledon Flowers 


by 
KENNETH R. SPORNE 


The Botany School, University of Cambridge 


Summary 


For more than 35 years, girdling vascular bundles have been known to occur in the 
flowers of species belonging to nine families of dicotyledons. Further families are now added 
to the list, bringing the total to twenty. The occurrence of girdling bundles does not appear 
to have any special taxonomic or phylogenetic significance. Vascular patterns with girdling 
bundles are illustrated for members of eleven families. 


The purpose of this paper is to draw attention to a phenomenon which is 
more widespread among dicotyledons than has hitherto been realized, namely, the 
Occurrence within the floral receptacle of a horizontal girdling vascular bundle 
which connects the vascular bundles supplying the perianth members. 


The term “‘girdling vascular bundle’’ was used by Saunders (1939) to describe 
such lateral interconnections in species belonging to the Cistaceae, Combretaceae, 
Lythraceae, Melastomataceae and Onagraceae. In four other families (Campanu- 
laceae, Hydrocaryaceae, Rubiaceae and Valerianaceae) she mentioned lateral con- 
nections but did not refer to them as girdles. To judge from her books, and from 
the references quoted therein, Saunders (1939) must have looked at representatives 
of at least 168 families of dicotyledons. Having examined representatives of more 
than 150 families myself, I have been able to add a further eleven to the list of 
those with girdling bundles. Three of these (Leguminosae, Tropaeolaceae and 
Violaceae) have already been briefly described (Sporne, 1974). The other eight 
families are Begoniaceae, Caricaeae, Ericaceae, Flacourtiaceae, Gentianaceae, 
Loasaceae, Stylidiaceae and Tiliaceae, which bring to twenty the total number of 
families in which this phenomenon has been recorded. 


As will subsequently become apparent, some distinction needs to be made 
between those girdles in which both the sepals and the petals are involved and 
those in which the petals alone are involved or the sepals alone. It is proposed to 
call the first type “‘composite girdles’’ and the second type either “‘simple corolla 
girdles” or “‘simple calyx girdles’, respectively. 


Vascular connections between the sepals and the petals in Campanula and 
Lobelia were mentioned by Henslow (1888), but the details of his description were 
not correct. Thus, in Campanula medium L., he stated that the vascular bundle 
intended for a sepal branches before reaching it and sends off two cords, one for 
each petal alternating with it, ‘‘so that each petal receives two cords, one from each 
adjacent sepal — a most unusual condition of things, for petals have almost 
invariably their own cords issuing from the pedicel.” If this description were correct 
it would, indeed, be unusual, for I know of only one example of a flower whose 
petals derive their entire vascular supply from that of the sepals, viz. Viola (Sporne, 
1974, fig. 52C). 


Plate 1 is a photograph, taken in the late Autumn, of an old flower of 
Campanula carpatica Jacq. At this time in the year, the soft tissues of the flower 
have rotted away, leaving just the vascular skeleton. The crown-like composite 
girdle is clearly visible. Fig. 1 is a stylized vertical projection of the vascular system 
in Campanula rotundifolia L., (omitting the supply to the gynoecium). Three 


165 


166 Gardens’ Bulletin, Singapore — XX1IX (1976) 


vascular bundles enter the base of the flower and branch, somewhat irregularly, in 
the wall of the inferior ovary, until near the top there are ten trunk bundles. Of 
these, five are on the sepal radii and, giving rise to the five stamen bundles (A), 


Ke cK 


I : 


« Fig. 1. Campanula rotundifolia L. 
a Fig. 2. A, Fuchsia fulgens Mog. and 
. Sessé ex DC. 


B, Epilobium angustifolium 
Tn 


Fig. 3. A, Circaea lutetiana L. 
B, Valeriana officinalis L. 


Girdling vascular bundles 167 


are continuous with the sepal mid-ribs (K). The other five trunk bundles are on 
the petal radii and continue into the petals, giving both the petal mid-rib (C) and 
the petal laterals (C’). Before the petal supply becomes distinct, however, all ten 
trunk bundles become connected by a horizontal girdle. It is from this girdle, and 
not from the sepal mid-rib, that the sepal laterals (K’) have their origin. A similar 
composite girdling bundle has been figured by Mabberley (1973) for Lobelia 
stricklandiae Gilliland. 


Fig. 2 illustrates the vascular system of two members of the Onagraceae, 
namely, Fuchsia fulgens Mog. and Sessé ex DC. and Epilobium angustifolium L. 
(Note that here, as in all the other illustrations, the vascular supply to the ovules 
and to the style is omitted.) In each of these two genera, there are eight trunk 
bundles in the wall of the inferior ovary, and a stamen bundle arises as a branch 
from each. They then become connected by a horizontal girdle which, in Fuchsia, 
is below the level of origin of the sepal and petal lateral bundles. In Epilobium, 
however, these lateral bundles have their origin in the girdle itself. Circaea lutetiana 
L. (Fig. 3A) also belongs to the Onagraceae, but has a much smaller flower than 
either Fuchsia fulgens or Epilobium angustifolium, yet it too has a horizontal girdle. 
There are four trunk bundles in the wall of the ovary, corresponding to the two 
sepals and the two petals, respectively. Each sepal receives five bundles, of which 
the laterals (K’ and K”) are derived from the girdle. The petal laterals (C’”) are, 
however, independent of it, as in Fuchsia fulgens. 


Valeriana officinalis L. (Fig. 3B), also has a very small flower. Its calyx is 
represented merely by about twelve curled teeth, which receive no vascular supply 
at all. Six trunk bundles run up in the wall of the inferior ovary; two of them fork, 
to provide the total of eight needed for the five petals and the three stamens, and 
then a horizontal girdle is formed, for which the term “simple corolla girdle’ is 
appropriate. 

Plate 2 illustrates the im- 
portance of clearing tech- 
niques when studying floral 
vascular systems. A_hori- 
zontal slice through the 
apex of the inferior ovary 
of Loasa vulcanica André, 
was boiled for a few se- 
conds in lactic acid (Sporne, 
1948) and was then photo- 
graphed by _ transmitted 
light. The vascular bundles 
show up as a silhouette, in 
which the horizontal com- 
posite girdle is clearly visi- 
ble. A structure as complex 
as this would have been 
very difficult to envisage 
from a study of a series of 
microtome sections. Fig. 4 
is a diagrammatic interpre- 
tation, based on_ several 
slices cut at slightly diffe- 

Fig. 4. Loasa vulcanica André. rent levels. Opposite each 
: of the five sepals there 
is a petaloid scale, receiving three vascular bundles (S and S’) and inside each 
scale there are two staminodes (ST). The stamens (A) are in groups opposite the 
five petals. The sepal lateral (K’) and the adjacent petal lateral (C’) arise con- 
jointly from the petal trunk bundle at a level slightly below that of the girdle. 


168 Gardens’ Bulletin, Singapore — X XIX (1976) 


Fig. 5 shows part of the receptacular vascular system in Mentzelia lindleyi 
Torr, & Gray, which belongs to the same family as Loasa, namely the Loasaceae. 
A portion of the receptacle 
was opened out flat and 
viewed from inside, after 
being cleared in lactic acid. 
The vascular system is 
strikingly different from 
x that of Loasa for, instead 
of a single girdling bundle, 
there is an anastomosing 
system connecting the sepal 
and petal trunk bundles 
and from it the stamens 
receive their vascular 
supply. A similar arrange- 
ment occurs in Mentzelia 
gronoviifolia Fisch, & 
Mey. Clearly, it would be 
unwise to generalize, on 
the basis of one genus 
within a family, about the 
occurrence of _ girdling 
bundles, for one can scarce- 
ly describe Mentzelia as 
having a girdle. 
This is true also of various members of the Cucurbitaceae. Thus, in the edible 
cucumber, Cucumis sativus L., there are ten trunk bundles connected by a network 
of smaller bundles, while the vascular network of Luffa cylindrica (L.) M. Roem., 


is even more noticeable, especially after it has been retted to produce the familiar 
bathroom loofah. The 


Cucurbitaceae can scarcely . Ff 

be said to have a vascular 6 a ae - 

girdle even though, from 

a physiological point of 

view, the vascular connec- 

tions may be directly com- ! 

parable. 
Stylidium graminifolium 

Sw. ex DC, belonging to 

the Stylidiaceae, raises a 

similar problem. Running 

up in the wall of the in- tf. \. 

ferior ovary, there are ten AY AIK ; 

trunk bundles (Fig 6), § $$$$$-§_ QPS A- ae ; 

some of which are connect- 

ed by horizontal bundles, ms 

while others are connected 

only by obliquely running | 

bundles. Perhaps Stylidium coc ¢ ; 


should be described as Fig. 6. Stylidium graminifolium Sw. ex DC. 
having only a partial girdle. broken line represents a nectary.) 


Fig. 5. Mentzelia lindleyi Torr. & Gray. 


Girdling vascular bundles 


We ah aa <" 


7 : 


B 


Fig. 7. Begonia evansiana Andr. A, staminate flower. 
B, pistillate flower. 


169 


The examples 
quoted so far have 
all been of herma- 
phrodite _ flowers. 
Begonia evansiana 
Andr. has _ uni- 
sexual flowers, and 
there is a well de- 
veloped horizontal 
girdle in the pistil- 
late flower, but 
only a partial one 
in the  staminate 
flower. In each, 
there are two se- 
pals and two petals. 
Fig 7A shows how, 
in the staminate 
flower, there are 
eight trunk bundles 
of which two lead 
directly into the 
sepal_ mid-ribs, 
while the remain- 
ing six become in- 
volved in two semi- 
circular partial 
girdles opposite 
the petals. The 
pistillate flower 
(Fig. 7B) has six 
trunk bundles in 
the wall of the in- 
ferior ovary which 
are connected by a 
complete horizontal 
composite _ girdle, 
from which petal 
laterals as well as 
sepal laterals ori- 
ginate. 


Girdling bundles 
are more likely to 
occur in flowers 
where the perianth 
members are whorl- 
ed, or even con- 
nate, rather than 
in those with 


spirally arranged 


perianth members. It is not surprising, therefore, that many examples of girdling 
bundles are found in flowers with inferor ovaries, where adnation, as well as conna- 
tion may have occurred as a result of ‘‘intercalary concrescence”’ (a term suggested 
by Stebbins, 1974, which avoids the ambiguities of ‘“‘fusion’’). However, there are 


170 Gardens’ Bulletin, Singapore — XX1X (1976) 


also several families with superior ovaries whose perianths receive their supply 
from girdling bundles. Such an arrangement has been described (Sporne, 1974) for 
Phaseolus, in the papilionate section of the Leguminosae. It is also to be found in 
Cassia floribunda Cav., in the caesalpinioid section of the family (Fig. 8A). Ten 
trunk bundles enter the base of the flower, each giving rise to a branch supplying 
either a stamen (A) or a staminode (ST). They then become connected by a horizon- 
tal girdle, from which the sepal lateral bundles (K’ and K”) have their origin. In 
passing, it should be noticed that the vascular bundles supplying the three lower- 
most stamens are peculiar in having a hollow cylinder of xylem. 

Among the Ericaceae, Rhododendron ponticum L., has a well developed 
composite girdle. Ten trunk bundles radiate from the central cylinder. As they run 
horizontally in the disc-shaped receptacle, they each give off a stamen bundle and 
then all ten bundles are united by a horizontal girdle, from which the sepal laterals 
have their origin. 

Fig. 9 (taken from Sporne, 1974, fig. 52A) illustrates the vascular system in 
Tropaeolum minus L. (The stamen supply is independent of the perianth supply 
and has, therefore, been omitted.) In this member of the Tropaeolaceae, there are 
ten trunk bundles in the base of the flower, of which three run the full length of 
the spur and back again. All ten are then connected by a girdle, from which the 
sepal laterals have their origin. 


In Sparmannia africana L. f., belonging to the Tiliaceae, eight trunk bundles 
enter the base of the flower, four opposite the sepals and four opposite the petals. 
Despite the fact that the sepal bundles turn outwards at a much lower level than 
do the petal bundles, they all become united by a horizontal girdle, from which the 
sepal laterals have their origin. 

Fig. 8B is of Heterocentron roseum 
A. Br. & Bouché, belonging to the 
Melastomataceae. Although the ovary is 
superior, it lies at the bottom of a cup- 
shaped receptacle. Eight trunk bundles 
run up in this receptacle, each giving off 
a stamen trace before becoming linked 
by a composite girdle. This is not the only 


Fig. 8. A, Cassia floribunda Cav. 
B, Heterocentron roseum A. 
Br. and Bouché. 

Fig 9. Tropaeolum minus L. (The 
broken lines represent the 
spur.) 


i 


Girdling vascular bundles 


171 


link, however, for there are some anastomosing bundles in addition, below the level 


of the girdle. 


Passiflora quadrangularis L. has a similar anastomosing network, but none of 
the connections is sufficiently large to justify the term “girdle’’. This arrangement 


K a 


10 ‘ 


Sie 


, 


B 


Fig. 10. A, Blackstonia perfoliata 
(L.) Huds. 


B, Chironia linoides L. 


is therefore equivalent to that in the 
Cucurbitaceae. Neither Passifloraceae nor 
Cucurbitaceae qualify for inclusion among 
those families with girdling bundles, as 
defined in this paper. 

Fig, 10 illustrates two genera belong- 
ing to the Gentianaceae, one of which has 
a simple calyx girdle, while the other is 
completely without any lateral connec- 
tions. The flower of Blackstonia perfo- 
liata (L.) Huds., illustrated in Fig. 10A, 
was one with eight sepals. Each received 
a mid-rib (K) and lateral veins (K’); and 
each pair of adjacent laterals was joined 
by a short bridging bundle, so as to pro- 
duce a “zig-zag” girdle. Chironia linoides 
L. (Fig. 10B) has pentamerous flowers in 
which the sepal supplies are completely 
independent of each other. Centaurium 
minus Moench, also belonging to the 
Gentianaceae, is variable in that bridges 
between adjacent sepal laterals are some- 
times present and sometimes absent. 


In Phyllobotryon spathulatum Muell. 
Arg., belonging to the Flacourtiaceae, the 
vascular supply to the three sepals is 
completely separate from that to the three 
petals, yet there are lateral connections 
in each system, Fig. 11A shows the calyx 
system, in which lateral connections form 
a partial girdle. Fig. 11B shows the 
corolla system, in which there are merely 
a few random interconnections. 


<7 
AS 


Fig. 11. Phyllobotryon spathulatum Muell. Arg. A, calyx. B, corolla. 


172 Gardens’ Bulletin, Singapore — XX1X (1976) 


The most remarkable vascular system that I have seen is that of Carica papaya L., 
illustrated in Fig. 12, The flowers are pentamerous and unisexual; and the perianth 
members derive all their vas- 
cular supply from five trunk 
bundles. However, the way in 
which this happens in the 
staminate flowers is strikingly 
different from that in the pistil- 
late flowers. Fig. 12A illustra- 
tes the vascular pattern of a 
staminate flower, in which 
there is a complete and simple 
calyx girdle, each sepal receiv- 
ing a midrib (K) and two 
lateral veins (K’). The trunk 
bundle to each petal has its 
origin, not independently from 
the central cylinder, but runs 
for a short distance conjointly 
with a sepal trunk bundle; ran 
then, on becoming separate, it 
moves laterally on to a diffe- 
rent radius. In the pistillate 
flower, illustrated in Fig. 12B, 
there is some variability, but 
mostly the petal trunk bundles C 
arise conjointly with sepal 
trunk bundles, as in the stami- 
nate flower. However, the 
sepals receive many veins, the 
number varying from sepal to . 
sepal, and only a partial girdle 
is formed. In passing, atten- BZ 
tion must be drawn to the 
stamen supply in the staminate N 
flowers. The particular flower 
illustrated in Fig. 12A had five 


trunk bundles, which became B 
connected by a partial girdle 

from which the ten stamen Fig. 12. Carica papaya L. 

bundles had their origin (but A, staminate flower. 

the exact details vary from B, pistillate flower. 


flower to flower). 

What the significance may be of girdling bundles in floral vascular systems is 
not easy to discern. There have always been two schools of thought, one which 
holds that the course taken by vascular bundles is of great phylogenetic significance 
and the other which holds that vascular bundles develop where and when there is 
a physiological need. To those who hold the former view, Professor Corner has 
been heard to say “‘Go and look at a loofah’, for of course it would be hard to 


justify the claim that each and every strand in such a network is of phylogenetic — 
significance. Yet a reticulum, if described as such, might well be of phylogenetic — 
significance, for it may fulfil a physiological need imposed by the large size of the — 


fruit, which itself is of phylogenetic significance. Just as a reticulum may fulfil a 
need, so indeed may a girdling bundle, in providing alternative paths of conduction, 
analogous to closed vascular networks in stems. 


Plate 1. (above) Loasa vulcani- 
ca André., showing 
composite girdle. x 20. 


Plate 2. (below) Campanula 
carpatica Jacq. Vas- 
cular skeleton of 
flower. x 3. 


a4 yk 


ia “4 


AL RSE a 
te Ry 


ie * 


Girdling vascular bundles 173 


Too few examples have, so far, been described for any taxonomic significance 
to have come to light. Not only do many families of dicotyledons remain to be 
investigated, but so also do other species within those families which have been 
examined. We have, as yet, little idea of the variability that may exist from flower 
to flower on a single plant, or from individual to individual within a species. 
Summarizing our knowledge to date, one can say that girdling bundles occur in 
some members of six families in the Violales (Begoniaceae, Caricaceae, Cistaceae, 
Flacourtiaceae, Loasaceae and Violaceae), five in the Myrtales (Combretaceae, 
Hydrocaryaceae, Lythraceae, Melastomataceae and Onagraceae), two in the 
Campanulales (Campanulaceae and Stylidiaceae) and one family in each of the 
following: Dipsacales (Valerianaceae), Ericales (Ericaceae), Gentianales (Gentian- 
aceae), Geraniales (Tropaeolaceae), Malvales (Tiliaceae) and Rosales (Leguminosae). 
In the taxonomic scheme of Cronquist (1968), these orders are placed in the 
Dilleniidae, Rosidae and Asteridae. There is none in the Magnoliidae, Caryophy!l- 
lidae or Hamamelidae. 


The families in which girdling bundles occur range from very primitive to 
very advanced. Thus the Flacourtiaceae have an advancement index of 22% 
(Sporne, 1969), while the Dipsacaceae are almost at the other extreme, with one 


of 94%. It is clear, therefore, that girdling bundles are poor indicators of evolution- 
ary Status. 


One interesting fact emerges from a study of the vast literature dealing with 
floral vascular systems, and this is that morphologists who rely on microtome 
sections often fail to notice girdling bundles. A plea is, therefore, made for more 
frequent use of clearing techniques, for I have no doubt that those who use them 
will find that girdling bundles are much more widespread in their occurrence than 
has been realised. Then, eventually perhaps, their significance (be it taxonomic or 
phylogenetic) will become apparent. In the meantime, it would be wise to follow 
the advice of Carlquist (1970) and refrain from allowing interpretations to intrude 
into what should be purely descriptive work. 


Bibliography 


CARLQUIST, S. 1970. Towards acceptable evolutionary interpretations of floral 
anatomy. Phytomorphology 19: 332-362. 


CRONOQUIST, A. 1968. The evolution and classification of flowering plants. 
Nelson, London. 


HENSLOW, G. 1888. The origin of floral structures through insect and other 
agencies. Kegan, Paul and Trench, London. 


MABBERLEY, D. J. 1973. The pachycaul species of Senecio and Lobelia in 
Africa. Unpublished Ph.D. dissertation, University of Cambridge. 


SAUNDERS, E. R. 1937 and 1939. Floral Morphology: a new outlook, with special 
reference to the interpretation of the gynaecium. 2 Vols. Heffer, Cambridge. 


SPORNE, K. R. 1948. A note on a rapid clearing technique of wide application. 
New Phytol. 47: 290-291. 


— 1969. The ovule as an indicator of evolutionary status in angio- 
sperms. New Phytol. 68: 555-566. 


—————— 1974. The morphology of angiosperms. Hutchinson, London. 
STEBBINS, G. L. 1974. Flowering plants: evolution above the species level. 
Arnold, London. 


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Corner’s Architectural Model 


by 
F. HALLE & D. J. MABBERLEY 
Institut de Botanique Botany School, Oxford 
Montpellier, France England 


Vegetatively unbranched trees with indeterminate apical growth and lateral 
sexuality belong to ‘Corner’s Model’, as previously defined (Hallé & Oldeman, 
1970). The papaya tree and the oil palm are familiar examples of this strange and 
probably very old strategy of growth. The monoaxial trunk, often thick in its 
primary tissues, is built by the activity of a single apical meristem; the leaves are 
large, often compound, and the internodes are short. Growth may be continuous 
or rhythmic; cauliflory is frequent in the Angiosperm examples, From an ecological 
point of view, they are mainly treelets of the tropical rain-forest undergrowth. 


Although flowering before branching, these trees are not necessarily unbranch- 
ed throughout their lives, e.g. old papaya trees produce branches from buds on the 
trunk; see also Plate I. This repetition of the original model, for each new branch 
behaves as did the first axis, is the ‘réitération’ of Oldeman (1974). Again, damage 
to the apex sometimes leads to the death of some species, e.g. Cyanea carlsonii 
Rock (Degener, Degener & H6érmann, 1969), but others can recover, as their 
axillary buds grow out, giving a branched tree. 


Corner’s Model is important in the tropics, as it occurs in nearly all the larger 
families of flowering plants. A list of 67 trees was published in 1970 by Hallé & 
Oldeman; now more than a hundred species are known to be monoaxial, but the 
present list is likely to expand rapidly in the coming years, with the increasing 
interest in, and knowledge of, tropical tree architecture. 


Taxonomic Distribution 


The list below includes that of Hallé & Oldeman (1970: 21-5; 135), examples 
from which are indicated by an asterisk; bibliographic references to these are to 
be found in the original list. 


DICOTY LEDONS 


ANACARDIACEAET 
Semecarpus magnifica K. Schum., New Guinea (F. Hallé, 1974) 
Semecarpus sp., Malaysia, Mabberley 1668 (Plate 1) 
*Trichoscypha ferruginea Engl., Equatorial Africa 


BALANOPACEAE 
Balanops pancheri Baill., New Caledonia (J. M. Veillon, ined.) 


BERBERIDACEAE 


Mahonia bealei Carr., China; ‘‘Les Cédres’’ Botanical Garden, Saint-Jean- 
Cap-Ferrat, France. 1973 


} Harpephyllum caffrum Bern. exkr., grown from seed, has flowered at Oxford without 
branching, while this paper was in press. 


175 


176 Gardens’ Bulletin, Singapore — XX1X (1976) 


BIGNONIACEAE 


Colea lantziana Baill., Madagascar, Tsimbazaza Botanical Garden, Tanana- 
rive. 1974 


Colea nana Perrier, Madagascar; Tsimbazaza Botanical Garden, Tananarive, 
1974 


Colea sp., Madagascar, Mabberley 822 (1971) 


CAMPANULACEAE — LOBELIOIDEAE 
Brighamia rockii St. John, Hawaii (St. John, 1969) 
Cyanea aspleniifolia (Mann) Hillebr., Hawaii (Rock, 1919) 
Cyanea carlsonii Rock, Hawaii (Degener, Degener & Hérmann, 1969) 
Cyanea giffardii Rock, Hawaii (Rock, 1919) 
Delissea undulata Gaud., Hawaii (Rock, 1919) 


CARICACEAE 


*Carica papaya L., Central America, now pantropical 
*Carica sp., French Guyana 


COMPOSITAE 
*FEspeletia spicata Sch. Bip. ex Wedd., S. American mountains 


CON NARACEAE 
*Jollydora duparquetiana (Baill.) Pierre, Equatorial Africa 
CU NONIACEAE 
Cunonia macrophylla Brongn, & Gris., New Caledonia (J. M. Veillon, ined.) 


EUPHORBIACEAE 
* Agrostistachys borneensis Becc., Malaya and Borneo 
* Agrostistachys sessilifolia Pax & Hoffm., Malaya (see F. Hallé, 1971) 
Cleidion lasiophyllum Pax & Hoffm., New Caledonia, (J. M. Veillon, ined.) 
Euphorbia ankarensis Boiteau, Madagascar (G. Cremers, ined.) 
Euphorbia bupleurifolia Jacq., South Africa (G. Cremers, ined.) 


Euphorbia lophogona Lam., Madagascar; ‘‘Les Cédres” Botanical Garden, 
Saint-Jean-Cap-Ferrat, France, 1973 


Euphorbia moratii Rauh, Madagascar (G. Cremers, ined.) 
*Pycnocoma angustifolia Prain, West Africa (see F. Hallé, 1971) 
FLACOURTIACEAE 


Phyllobotryon spathulatum Muell, Arg., (including *P, soyauxianum Baill.) 
Equatorial Africa (Richards, 1952; Letouzey, Hallé and Cusset, 1969) 


GERANIACEAE 

Geranium canariense Reuter, Canary Islands (Yeo, 1970) 
GESNERIACEAE 

Boea lanata Ridl., Malaysia (Burtt, 1964) 
LAURACEAE 

Litsea ripidion Guill., New Caledonia (J. M. Veillon, ined.) 


4 
¢ 
, 


berley 1668 — Sepilok Forest Reserve, Sabah, 


ab 
8 May 1974 


Semecar pus sp., M 


Malaysia 


Plate I. 


Corner’s Architectural Model 177 


LECYTHIDACEAE 
Barringtonia calyptrocalyx K. Schum., New Guinea (F. Hallé, 1974) 
*Grias sp., Brazil 


LEGU MINOSAE-MIMOSOIDEAE 
Pithecellobium hansemanii (F. Muell.) Mohl, New Guinea (F. Hallé, 1974) 


LEGU MINOSAE-PAPILIONOIDEAE 
Angylocalyx oligophyllus Bakf., Tropical Africa (Mangenot, 1975) 
Sophora sp., New Caledonia (J. M. Veillon, ined.) 


MALVACEAE 


Goethea strictiflora Hook., Brazil; J. N. Maclet Botanical Garden, Tahiti, 
French Polynesia, 1973 


MELIACEAE 
Aglaia sp., Malaysia, Mabberley 1699 (1974) 


Chisocheton macranthus (Merr.) Airy Shaw, Malaysia, Mabberley 1718 
(1974) 


Chisocheton medusae Airy Shaw, Malaysia, Mabberley 1680 (1974) 
Chisocheton polyandrus Merr., Malaysia, Mabberley 1688 (1974) 
Chisocheton princeps Hemsl., Malaysia, Mabberley 1561 (1974) 
Chisocheton setosus Ridl., Malaysia, Mikil SAN 30162 (1963) 
Dysoxylum urens Val., Indonesia; Bogor Botanical Garden, 1972 
*Guarea richardiana A, Juss., French Guyana 


MENISPERMACEAE 
Penianthus sp. Gabon, N. Hallé 4056 (1966) 


MorACEAE 
*Ficus theophrastoides Seem., Solomon Islands 


MYRSINACEAE 
Oncostemon sp., Madagascar (J. L. Guillaumet, ined.) 
Rapanea grandifolia S. Moore, New Caledonia (J. M. Veillon ined) 


Tapeinosperma pachycaulum St. & Whitm., Solomon Islands (Stone & 
Whitmore, 1970) 


Tapeinosperma cristobalense St. & Whitm., Solomon Islands (Stone & 
Whitmore, 1970) 


Tapeinosperma sp., New Ireland (M. Coode, ined.) 
Gen, dub., Rondonia, Brazil, F. Hallé 2351 (1975) 


MYRTACEAE 
Jambosa acris Panch., New Caledonia (J. M. Veillon, ined.) 


OCHNACEAE 
*Campylospermum duparquetianum (Baill.) Van Tiegh., Tropical Africa 
*Campylospermum sacleuxii (Van Tiegh.) Farron, Tropical Africa 
*Campylospermum subcordatum (Stapf) Farron, Tropical Africa 
*Campylospermum zenkeri (Engl.) Farron, Tropical Africa 


178 Gardens’ Bulletin, Singapore — XXIX (1976) 


PITTOSPORACEAE 
*Pittosporum ceratii Guill., New Caledonia (J. M. Veillon ined.) 


PROTEACEAE 
Hicksbeachia pinnatifolia F. Muell., Australia; Sydney Botanical Garden, 1972 
Macadamia angustifolia R. Virot, New Caledonia (J. M. Veillon, ined.) 


RUBIACEAE 
*Bertiera simplicicaulis N, Hallé, Equatorial Africa 
Bikkia macrophylla K. Schum., New Caledonia (J. M. Veillon, ined.) 
Captaincookia margaretae N. Hallé, New Caledonia (N. Hallé, 1973) 
Coffea macrocarpa A. Rich., Mauritius (G. Mangenot, ined.) 
Gardenia conferta Guill., New Caledonia (J. M. Veillon, ined.) 
*Pentagonia gigantifolia Ducke, Peru 
Pseudomantalania macrophylla J. F. Leroy, Madagascar (Leroy, 1973) 


SAPINDACEAE 
*Chytranthus longiracemosus Gilg ex Radlk., Tropical Africa 
*Chytranthus mangenotii N. Hallé & Assi, Tropical Africa 
*Chytranthus pilgerianus (Gilg) Pellegr., Gaboon 
*Chytranthus welwitschii Pellegr., Gaboon 
Deinbollia sp., Banco Arboretum, Ivory Coast, 1967 


Jagera serrata Radlk., Papua New Guinea, Frodin & Mabberley UPNG 4305 
(1974) 


*Placodiscus bancoensis Aubr. & Pellegr., Ivory Coast 
*Radlkofera calodendron Gilg, Gaboon 


SAPOTACEAE 

*Delpydora gracilis A. Chev., West Africa 

*Delpydora macrophylla Pierre, Equatorial Africa 

Planchonella pronyensis Guill., New Caledonia (J. M. Veillon ined.) 
SIMAROUBACEAE 

*Brucea antidysenterica Lam., Ivory Coast 

*Eurycoma longifolia Jack, Malaysia 
SOLANACEAE : 

aff, Solanum, Acre, Brazil, F. Hallé 2352 (1974) | 


STERCULIACEAE 
*Chlamydocola chlamydantha (K. Schum.) Bodard, Tropical Africa 
*Cola buntingii Bak.f., West Africa 
*Cola caricaefolia (G. Don f.) K. Schum., West Africa 
*Cola mahoundensis Pellegr., Equatorial Africa 
Herrania albiflora Gaudot, Tropical America; Bogor Botanical Garden, 1972 
*Ingonia digitata (Mast.) Bodard, West Africa 
*Theobroma mariae K. Schum., Tropical America 
SYMPLOCACEAE | | 
Symplocos stravadioides Brongn. & Gris., New Caledonia (J. M. Veillon, ined.) 


Corner’s Architectural Model 179 


THEOPHRASTACEAE 
*Clavija lancifolia Desf., French Guyana 
*Clavija longifolia (Jacq.) Mez, Tropical America 


URTICACEAE 


Dendrocnide moroides (Wedd.) Chew, Australia; “‘Les Cédres’’ Botanical 
Garden, Saint-Jean-Cap-Ferrat, France, 1975 


Obetia radula (Bak.) B. D. Jackson, Madagascar, Mabberley 752 (1971) 


VERBENACEAE 
Oxera coriacea Dubard, New Caledonia, J. M. Veillon 2574 (1973) 


VIOLACEAE 
* Allexis cauliflora (Oliver) Pierre, Equatorial Africa 
Neckia serrata Korth., Indonesia, (Boerlage & Koorders, 1901) 


MONOCOTY LEDONS 


AGAVACEAE 
*Nolina recurvata Hemsl., Mexico 
PALMAE (Corner’s is the main architectural model within the family — see Corner 


(1966) and Whitmore (1973). The following is a short list of typical 
examples) 


Borassus aethiopum Mart., Tropical Africa 
*Cocos nucifera L., pantropical 


Dypsis hildebrandtii Becc., Madagascar; Tsimbazaza Botanical Garden, 
Tananarive, 1971 


*Elaeis guineensis Jacq., Tropical Africa 

Lodoicea maldavica (Gmel.) Pers., Seychelles 

*Mauritia flexuosa Benth., Hook.f. Tropical America 
Oenocar pus distichus Mart., Brazil 

*Phytelephas macrocarpa Ruiz & Pav., Colombia 

* Roystonea oleracea O. F. Cook, Central America 
Verschaffeltia splendida H. Wendl., Seychelles 


PANDANACEAE 
Pandanus danckelmannianus K. Schum., Solomon Islands (Stone, 1972) 
Pandanus princeps B. C. Stone, Madagascar (Stone, 1970; Guillaumet, 1973) 


OTHER VASCULAR PLANTS, LIVING OR FOSSIL 


FERNS 
*Caulopteris sp., fossil 
*Hagiophyton sp., fossil 
*Megaphyton sp., fossil 
*Psaronius sp., fossil 
*Alsophila australis R.Br., Tasmania 


180 Gardens’ Bulletin, Singapore — X XIX (1976) 


*Cyathea camerooniana Hook., Tropical Africa 
*Dicksonia sp., Melanesia 
*Thamnopteris schlechtendalii (Eichwald) Brongniart, fossil 


PTERIDOSPERMS 
*FEospermatopteris sp., fossil 
*] yginopteris oldhamia (Binney) Potonie, fossil 
*Medullosa noei Steidtmann, fossil 


CYCADS 
*Cycadeoidea jenneyana Ward, fossil 
* 2 Cycas circinnalis L., South East Asia 
* 2 Cycas revoluta Thunb., Asia 
* Encephalartos laurentianus De Wild., Zaire 
*Palaeocycas integer (Nath.) Florin, fossil 
*Williamsonia sewardiana Sahni, fossil 


References 


BOERLAGE, J. G. & S. H. KOORDERS. 1901. Tabula LXXVI. Neckia serrata 
Korth. Icon. Bogor. 4: 1-3. 


BURTT, B. L. 1964. Angiosperm taxonomy in practice. Syst. Assoc. Publ. 
6: 5-16. 


CORNER, E. J. H. 1966. The Natural History of Palms. Pp. 393. Weidenfeld & 
Nicholson, London. 


DEGENER, O, I. DEGENER & H. HORMANN. 1969. Cyanea carlsonii Rock 
and the unnatural distribution of Sphagnum palustre L. Phytologia 19: 1-4. 


GUILLAUMET, J. L. 1973. Formes et développment des Pandanus malgaches. 
Webbia 28: 495-519. 


HALLE, F. 1971. Architecture and growth of tropical trees exemplified by the 
Euphorbiaceae. Biotropica 3 (1) : 56-62. 


F. 1974. Architecture of trees in the Rain Forest of Morobe District. 
New Guinea. Biotropica 6 (1) : 43-50. 


HALLE, F. & R. A. A. OLDEMAN. 1970. Essai sur Vlarchitecture et la 
dynamique de croissance des arbres tropicaux. Pp. 178. Masson éd., Paris. 


HALLE, N. 1973. Captaincookia, genre nouveau monotypique néocalédonien de 
Rubiaceae — Ixoreae. Adansonia 13 (1) : 195-202. 


LEROY, J. F. 1973. Sur Vorganisation et le mode de développment d’un trés 
remarquable ensemble naturel de Rubiacées-Gardéniées 4 Madagascar, C.r. 
hebd. Séanc. Acad, Sci. Paris 277: 1657-1659. | 


LETOUZEY, R., N. HALLE & G. CUSSET. 1969. Phyllobotryae (Flacourtia- : | 
ceae) d’Afrique Centrale; variations morphologiques et biologiques; | 
conséquences taxonomiques. Adansonia 9 (4) : 515-537. 


MANGENOT, G. 1957. Angylocalyx oligophyllus Bak. f. 1913. Icones Pl. afr. — 
4: 77. 


OLDEMAN, R. A. A. 1974. L’architecture de la forét Guyanaise. O.R.S.T.O.M., | 
Paris. 4 


Corner’s Architectural Model 181 


RICHARDS, P. W. 1952. The tropical rain-forest. Cambridge University Press. 


ROCK, J. F. 1919. A monographic study of the Hawaiian species of the tribe 
Lobelioideae family Campanulaceae. Mem. Bernice P. Bishop Mus. 7 (2): 
1-394. 


ST. JOHN, H. 1969. Monograph of the genus Brighamia (Lobeliaceae). Hawaiian 
Plant Studies 29. Bot. J. Linn. Soc. 62: 187-204. 


STONE, B. C. 1970. Observations on the genus Pandanus in Madagascar. Bot. 
J. Linn. Soc. 63: 97-131. 


1972. The genus Pandanus in the Solomon Islands with notes on 
adjacent regions. Malaysian J. Sci. 1 A: 93-132. 


STONE, B. C. & T. C. WHITMORE. 1970. Notes on the systematy of Solomon 
Islands plants and some of their New Guinea relatives. XI. Tapeinosperma 
(Myrsinaceae). Reinwardtia 8 (1) : 3-11. 


WHITMORE, T. C. 1973. Palms of Malaya. Pp. 148. Oxford University Press. 


YEO, P. F. 1970. Geranium palmatum group in Madeira and the Canary Isles. 
J. R. hort. Soc. 95: 410-414. 


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Where and When Might the Tropical Angiospermous Flora 
Have Originated? 


by 
RoBErRT F. THORNE 


Rancho Santa Ana Botanic Garden, Claremont, California 91711 


Summary 


The tropical angiospermous flora had its beginnings with the origin of the angiosperms 
in earliest Cretaceous time from some unknown, generalized gymnospermous ancestor, pro- 
bably a still unrecognized group of Mesozoic pteridosperms. Over most of early and middle 
Cretaceous time, the angiosperms, early split into dicots and monocots, gradually became 
more prominent in tropical and later in temperate floras, with evolution by late Cretaceous 
in part into extant families and genera. The facts of present and past angiosperm distribution 
still point to southeastern Asia and attendant archipelagoes as the primary centre of preserva- 
tion and probably the primary centre of origin of the most primitive living angiosperms. 
Other important centres for the development of the tropical angiosperm flora have been 
West Gondwanaland before its break-up, the upland shield areas of South America and 
Africa since their isolation from one another, Australasia, and to a much lesser extent the 
Greater Antilles and Mexican highlands. 


Introduction 


The origins of the angiosperms are still obscure. When, where, and from what 
ancestral group they originated are still matters of much speculation and disagree- 
ment. We are much better supplied with negative information than with positive 
facts due to the incomplete nature of the fossil record and the almost universal 
extinction of the earliest angiosperms and their probable ancestors. However, 
expanding knowledge about the class Angiospermae enables us to narrow down 
_ considerably our choice of answers. 


Antiquity of the Angiospermae 


The earliest guesses about the antiquity of the angiosperms were rather wild, 
ranging from the Cretaceous back at least to the Permian of late Paleozoic time. 
The earliest indisputable angiosperm remains, monosulcate angiosperm and tricol- 
pate pollen, appeared in the fossil record in Barremian and Aptian time of the 
Lower Cretaceous less than 130 million years ago (Doyle, 1969, 1973; Wolfe et al, 
1976). Earlier fossil remains claimed to be angiospermous have been eliminated 
from consideration as belonging to other vascular plant classes or as having come 
from more recent strata than those to which they were first assigned (Scott, Leopold. 
and Barghoorn, 1960; Scott et al, 1972). The complete absence of unequivocal 
angiosperm fossils from strata earlier than the Barremian, or possibly the Hauteri- 
vian, makes it gratuitous to assume a much earlier Jurassic or even Triassic origin 
for the angiosperms. 


Gradual Emergence of the Angiospermae 


Another myth like early Mesozoic origins that should be set aside permanently 
for the early angiosperms is that they burst full-bloom in great numbers and variety 
upon the Early Cretaceous scene. We have enough fossil floras analyzed now that 
we can say categorically that the angiosperms very slowly gained prominence in 


183 


184 Gardens’ Bulletin, Singapore — X XIX (1976) 


the world’s floras of gymnosperms and ferns and even more gradually evolved into 
groups recognizable as extant families and genera. About 15 million years of slow 
angiosperm evolution took place before diverse angiosperm floras, like the Dakota, 
Potomac, and Cheyenne Sandstone floras, came into prominence by Upper Albian 
time, perhaps 112 million years ago (Wolfe et al, 1976). Not until the Turonian and 
Senonian, 100 to 90 million years ago, were gymnosperm pollen and fern spores 
over-taken in abundance in the fossil record by angiospermous pollen. By late 
Senonian time, perhaps 70 million years ago, angiosperms had largely replaced the 
ferns and gymnosperms (Muller, 1970, Wolfe, 1974, Wolfe et al, 1976). Possibly 
modern orders had appeared some tens of millions of years earlier. Many modern 
families and most extant genera have not been recognised from the fossil record 
until Tertiary times in the last 65 million years, and many taxa still have no accept- 
able fossil record. 
Probable Angiosperm Ancestors 


Our knowledge of the morphology of various vascular plant classes has now 
enabled us to narrow down considerably those primitive vascular-plants groups 
that might have evolved into the early angiosperms. Pteridophytes, confers, ginkgoes, 
cycads, gnetophytes, and the extinct Cordaitales and Bennettitales have now been 
removed from consideration, largely because they are more specialized in certain 
features than those archaic angiosperms now generally regarded as the most primi- 
tive living flowering plants (Eames, 1961; Cronquist, 1968; Takhtajan, 1969). The 
most primitive gymnosperms, the extinct Pteridospermae or seed-ferns, still remain 
as possible ancestors because of their generally primitive characteristics and their 
great diversity. Most recently Stebbins (1974) has revived rather unconvincingly 
the hypothesis that the angiospermous ovule is homologous with the seed-bearing 
cupule of the advanced Mesozoic pteridosperm order Caytoniales. However, the 
fossil Caytoniales, like the eliminated vascular-plant groups listed above, appear to 
be too specialized to pass as angiosperm ancestors. It seems more likely that some 
little-known, or probably still unrecognized, unspecialized group of Mesozoic seed- 
ferns evolved very early in the Cretaceous into the first angiosperms. 


Where these long-extinct, unspecialized pteridosperms presumably evolved 
into recognizable angiosperms is also still controversial. At best, we can make an 
educated guess as to the probable centre of evolution of the Angiospermae by 
assembling what we know of the probable habitats of the earliest flowering plants 
and of fossil and extant distribution patterns of the most primitive living angio- 
sperms. 

Tropical Character of the Angiospermae 


Most angiosperm families are basically tropical in their adaptations and their 
geographic distribution. In an analysis of the 316 families accepted in my classifica- 
tion (Thorne, 1968, 1974), I have found 167 to have an exclusively or primarily _ 
tropical distribution, 106 a strong, or nearly equal, representation in both tropical 
and temperate zones, and only 43 an exclusively or largely temperate distribution. _ 
Of the 43 temperate families only four, Adoxaceae, Butomaceae s.s., Hippuridaceae, 
and Myzodendraceae, each represented by a single genus, are primarily cool temper- 
ate in distribution, although two subfamilies, Hectorelloideae and Tetrachondroideae — 
are essentially subantarctic in range. Every one of the 43 temperate families appears — 
to be related to families that are primarily tropical and that are less specialized in 
many features, i.e., more primitive. If additional subfamilies are totalled with the 
families, 314 families and subfamilies are primarily tropical, 204 both tropical and 
temperate, and only 101 primarily temperate. The tropical bias of the Angiospermae 
thus is readily evident, approximately three to one. The families generally con- 
sidered most primitive in the class are even more strikingly tropical. Analysis of the 
95 families of the relatively primitive superorders Annoniflorae, Theiflorae, Ruti- 
florae, and Hamamelidiflorae shows 57 primarily tropical and only 11 largely 
temperate, a ratio of more than five to one. 


Origin of the angiospermous flora 185 


Angiosperm megafossil evidence, according to Axelrod (1959, 1970) indicates 
that the first recognizable flowering plants appeared from equable, warmer uplands 
first in lower middle latitudes at the beginning of the Early Cretaceous (Neocomian 
time), where they made up a very small percentage of the total vascular plant 
flora. At that time they were unrepresented in the megafossil record at high lati- 
tudes. As Axelrod graphically shows, they appeared at higher latitudes in progres- 
sively younger rocks until by late Cretaceous time they had in great variety largely 
replaced pteridophytes and gymnosperms even at higher, temperate latitudes. By 
Aptian time according to megafossils, angiosperms were present south of the 
equator only in lower latitudes. By the end of the Early Cretaceous in the Albian 
stage they had reached 70° N latitude but were only beginning to appear at middle 
latitudes (45° S) in the southern hemisphere (Axelrod, 1959). Fossil pollen evidence 
seems to support only in the broadest way this apparent poleward migration of 
early angiosperms (Doyle, 1969; Brenner, 1976; Hopkins, 1974). From this data, we 
can infer that the Angiospermae evolved in tropical areas, probably north of the 
equator. 

Mesic Origins of the Angiospermae 


Perhaps even stronger than the fossil evidence are the inferences we can draw 
from extant archaic angiosperms, those relicts with vesselless xylem or with extremely 
primitive tracheid-like vessel elements that are long and narrow and have long 
scalariform perforation plates with usually more than 20 bars. These woody plants, 
like broad-leaved conifers, are essentially restricted to highly mesic sites with a 
minimum of seasonal water stress, primarily tropical montane forests or summer-wet 
temperate forests (Carlquist, 1975). This is a devastating argument against Stebbins’ 
recently enunciated hypothesis (1974) that the first angiosperms were shrubby plants 
that evolved in response to a stressful warm climate with distinct dry and wet 
seasons. It was only as the angiosperms evolved xylem with greater conductive 
efficiency that they were able to invade and radiate rapidly in the hot tropical 
lowlands with their wide fluctuations in soil moisture and high insolation, and the 
temperate forests with more seasonal water stress (Carlquist, 1975). The extreme 
plasticity of both dicotyledons and monocotyledons allowed many of them rather 
early in their evolution to adapt to extreme habitats and unusual life-styles (Hickey, 
1971; Doyle and Hickey, 1972; Doyle, 1973). 


Thus the evidence from both fossil and extant primitive angiosperms indicates 
that they arose in continuously moist, tropical or subtropical uplands. Indeed, it 
is in just such montane areas today that we find the great majority of the angio- 
sperms with a wide array of primitive features in flowers, pollen grains, seeds, and 
fruits as well as in stem anatomy, habit, and foliage. But we still have to decide 
which moist equable upland area is the probable original homeland of the primitive 
living Angiospermae. 


Possible Centre of Origin of Primitive Angiosperms 


Southeastern Asia and its adjacent archipelagoes have most often been sug- 
gested by plant geographers as not only the most important centre of preservation 
but also as the likely “cradle” of the Angiospermae (Takhtajan, 1957, 1969: Thorne, 
1963; Smith, 1970, 1973). Recently, however, the general acceptance of the theory 
of tectonic plate movement and sundering and floating apart of continents has 
caused some plant geographers to reconsider the problem with view to the suggested 
distribution of land masses during Cretaceous and early Tertiary times. Schuster 
(1972) and Raven and Axelrod (1974) favour Gondwanaland as the area from 
which the initial radiation of the angiosperms took place. The latter authors, on 
what often appears to be negative evidence, favour West Gondwanaland (South 
America and Africa as a unit), while claiming unconvincingly that the Oriental 
Region could not be the area of origin of the angiosperms because of its presumed 
composite Continental origin. 


186 Gardens’ Bulletin, Singapore — X XIX (1976) 


Oriental Region 


We should, therefore, examine the flora of the Oriental Region, which I define 
here as tropical southeastern Asia and the adjacent Indian-Western Pacific Ocean 
archipelagoes from Ceylon and Taiwan to tropical Queensland and Fiji. Few plant 
geographers would deny that this region has the world’s most varied flora. Though 
smaller than the Ethiopian and Neotropical Regions, it possesses indigenous repre- 
sentatives of 433 major angiospermous taxa (families and additional subfamilies), 
45 of them endemic, as compared to 366 major taxa, 38 endemic, for Madagascar 
and Africa south of the Sahara Desert, and 374, with 25 endemic, for all of South 
America including Fuegia. Among the most primitive angiosperms, the Annonales, 
Berberidales, Nymphaeales, and Hamamelidales, representation in the Oriental 
Region is even more overwhelming: 29 of 34 major annonalean, 15 of 18 berberi- 
dalean, 6 of 6 nymphaealean, and 11 of 11 hamamelidalean taxa. The same distribu- 
tion pattern with the most primitive members of the taxon restricted to the Oriental 
Region is repeated in major taxon after major taxon. Takhtajan (1969) has given 
many examples. Some of the additional tropical groups that appear to have evolved 
primarily in southeastern Asia are the thealean Dillenioideae, Actinidiaceae, Dip- 
terocarpaceae, Nepenthaceae, and Planchonioideae; Ericaceae; Symplocaceae; 
Rafflesioideae; Elaeocarpaceae; Ficus; Gonystylus; Cardiopteris; Rutaceae; 
Sabiaceae; Acer; Juglandineae; Fagales; Staphyleaceae; Daphniphyllineae; Cry- 
pteroniaceae; Astronioideae; Cyrtrandroideae; Rhizophoraceae; Cornineae (except 
Garrya); Caprifoliaceae; orchidaceous A postasiodeae and Cypripedioideae; Pan- 
danaceae; and Zingiberaceae. 


That the Oriental Region is of composite Continental origin may well be true. It is 
widely claimed that India-Ceylon split away from Africa and Madagascar at least 100 
million years ago, colliding with Asia 45 m. y. BP, and that Australia broke away 
from Antarctica about 49 m. y. BP, arriving in its present position near Indonesia 
some 15 m. y. BP (Raven and Axelrod, 1975). Assuming that this time-table is 
correct, even 15 million years is surely more than adequate time to explain the — 
widespread Indo-Malesian elements that dominate the rain-forest flora of tropical 
Queensland, New Guinea, and the other Melanesian islands. The flora of distinctive 
relicts of Australasia that Raven and Axelrod seem to attribute to Gondwanaland 
are more likely Oriental derivatives which have found a refuge in the isolated 
islands and highlands of Australasia. Degeneria, Galbulimima, and Eupomatia are 
very close relatives of the Magnoliaceae, of which all 12 genera and most of the 
perhaps 215 species are represented in mainland southeastern Asia or the Malay 
archipelago. The recently rediscovered Idiospermum of Queensland belongs to the 
Calycanthaceae (Thorne, 1974), whose other two genera, Calycanthus and Chimo- 
nanthus, are both represented in China. Amborella, Austrobaileya, and the 
Trimeniaceae have close relationships to the Calycanthaceae and to the Chloran- 
thaceae and Monimiaceae, both heavily represented in the Indomalesian area. 
Possibly the Winteraceae, with chief centres of variation in New Guinea and New 
Caledonia may be authochthonous relicts of Australasia but they have relatively 
close affinities with the Oriental Illiciineae and Magnoliineae. The only two 
hamamelidalean genera of Queensland, Ostrearia and Neostrearia of the Ham- 
amelidoideae, have undoubtedly reached northern Queensland, like Distyliopsis in | 
New Guinea, from southeastern Asia, where their probable two closest relatives / 
Embolanthera and Maingaya occur along with representatives of the other four | 
subfamilies and a total of 15 of the 27 hamamelid genera, 4 more being found in | 
temperate Asia. It is noteworthy that like the rain-forest angiosperm flora of New | 
Guinea, New Caledonia, and tropical Queensland, most of the insect, land snail 
oligochaete, avian, bat, and murid rodent faunas, at least of New Guinea and the 
tropical rain forests of Queensland, are derived from southeastern Asia or Malesia — 


Schodde and Calaby, 1972). For these reasons in my biogdbeskabindl subdivisio 
of the Pacific islands (1963) I treated New Guinea, the Bismarck, Admiralty, ar 


Origin of the angiospermous flora 187 


Solomon Islands, wet tropical Queensland, and New Caledonia as the Papuan and 
Neocaledonian subregions of the Oriental Region. I do not think a Gondwanic 
origin of Australia-New Guinea has had much impact upon the majority of angio- 
spermous elements of the tropical rain forests of Australasia. 


West Gondwanaland 


The importance of West Gondwanaland and other tropical areas in the evolu- 
tion of the tropical angiospermous flora must not be ignored, however. The Creta- 
ceous angiosperms, according to the fossil record, radiated evolutionarily and geo- 
graphically very widely and rapidly. Before West Gondwanaland disintegrated into 
the modern widely separate austral continents, it was probably the centre of origin 
of the tropical Annonineae; Scytopetalineae; Sapotineae; Euphorbiales; Geraniales: 
Caricineae; Hydnoraceae; Chenopodiineae; the rosalean Chrysobalanaceae, 
Connaraceae, Caesalpinoideae, Mimosoideae, and Podostemaceae; _lilialean 
Haemodoreae, Hypoxidoideae, Vellozioideae, and Iridaceae; Areciflorae; and 
Musaceae, among others. A longer list can be gleaned from Raven and Axelrod 
(1974), but it must be used with caution since they claim a Gondwanic origin for 
taxa that are and were apparently meagrely represented there if at all. 


South America 


After the break-up of Gondwanaland, the ancient shield areas of South 
America, especially the Guayana Highlands and Brazilian Planalto, appear to have 
contributed heavily to the development of such important tropical groups as the 
thealean Bonnetioideae, Pellicieroideae, Marcgraviaceae, Caryocaraceae, Sarra- 
ceniaceae, Quiinaceae, and Lecythidoideae; Theophrastaceae; cistalean Peridiscus, 
Leonioideae, and Loasaceae; Solanaceae; Goupia; Lissocarpaceae; tiliaceous 
Tetralicoideae and Neotessmannioideae; Houmirioideae,; Polygalineae; rutalean 
Dictylomatoideae, Spathelioideae, and Alvaradoideae; centrospermous Cactaceae, 
Rhabdodendraceae, and Coccoloboideae; rubiaceous Henriquezioideae; Marty- 
niaceae; Asteraceae; Cyclanthaceae; commelinalean Bromeliineae, Pontederiaceae, 
Juncaceae, Commelinineae, and Eriocaulineae; and zingiberalean Heliconioideae, 
Cannaceae, and Marantaceae. 

Africa 


On the other hand, Africa seems to have contributed somewhat less to the 
origins of the tropical flora, perhaps because of the floristic depauperization that 
Raven and Axelrod (1974) emphasize so strongly. Certainly of African-Madagascan 
origin are the thealean Scytopetalaceae, Sarcolaenaceae, Sphaerosepalaceae, 
Monotoideae, Dioncophyllaceae, and Napoleonoideae; Huacaceae; Barbeyaceae; 
Didymelaceae; simaroubaceous Kirkioideae and Balanitoideae; Melianthaceae: 
centrospermous Aizoaceae and Didiereaceae; rosalean Jollydoroideae, Montini- 
oideae, and Medusagynaceae; pittosporalean Brunineae; myrtalean Oliniaceae and 
Paenaeaceae; Pedaliaceae; Hoplestigmataceae; and lilialean Cyanastroideae and 
Geosiridoideae. 

Australasia 


Although Australasia seems to receive little credit as an important centre of 
evolution from Raven and Axelrod (1974), it has contributed significantly to the 
origins of the tropical angiosperm flora. Among other groups that had their primary 
development if not their origin in Australasia are the Winteraceae; Epacridaceac; 

; ceae; Stackhousiaceae; Akania, Gyrostemonaceae; rosalean Fscalloni- 
oideae, Cunoniaceae, and Davidsonia; Pittosporineae; Proteaceae; Casuarinaceae: 
myrtaceous Leptospermoideae; WHaloragaceae; lamialean Chloanthoideae and 
Prostantheroideae; liliaceous Xanthorrhoideae; Restionaceae; Centrolepidaceae, 
and the poaceous Micrairoideae. 


188 Gardens’ Bulletin, Singapore — XX1IX (1976) 


North America and Temperate Eurasia 


North America and temperate Eurasia appear to have contributed few major 
groups to the tropical angiospermous flora, despite their formerly rich tropical 
floras. The highlands of Mexico and the Greater Antilles may have contributed to 
the tropical flora Cyrillaceae, Polemoniaceae, Fouquieriaceae, Chitonioideae, 
Eriogonoideae, Crossosomataceae, Echeverioideae, Garryaceae, and the liliaceous 
Agavoideae. The total elimination of tropical elements from Europe removes that 
area from consideration until the fossil record of its tropical epochs is better known. 


LITERATURE CITED 


AXELROD, D. I. 1959. Poleward migration of early angiosperm flora. Science, 
N.Y. 130: 203-207. 


1970. Mesozoic paleogeography and early angiosperm history. Bot. 
Rev. 36: 277-319. 


BRENNER, G. J. 1976. Middle Cretaceous floral provinces and early migrations of 
angiosperms. Pp. 23-47. In C. B. Beck (Editor), Origin and Early Evolution of 
Angiosperms. Columbia Univ. Press, New York. 341 pp. 


CARLQUIST, S. 1975. Ecological Strategies of Xylem Evolution. Univ. Calif. 
Press. Berkeley, Los Angeles, London. 259 pp. 


CRONQUIST, A. 1968. The Evolution and Classification of Flowering Plants. 
Houghton Mifflin, Boston, 396 pp. 


DOYLE, J. A. 1969. Cretaceous angiosperm pollen of the Atlantic costal plain 
and its evolutionary significance. J. Arnold Arbor. 50: 1-35. 
1973. Fossil evidence on early evolution of the monocotyledons. 
QO. Rev. Biol. 48: 399-413. 


& L. J. HICKEY. 1972. Coordinated evolution in Potomac Group 
angiosperm pollen and leaves. (Abstract). Am. J. Bot. 59: 660. 


EAMES, A. J. 1961. Morphology of the Angiosperms. McGraw-Hill, New York, 
Toronto, London. 518 pp. 


EMERSON, A. E. 1955. Geographical origins and dispersions of termite genera. 
Fieldiana, Zool. 37: 465-521. 


GRESSITT, J. L. 1956. Some distribution patterns of Pacific Island faunae. Syst. 
Zool. 5: 11-32, 47. 


1961. Problems in the zoogeography of Pacific and Antarctic insects. 
Pacif. Insects Monogr. 2: 1-94. 


HICKEY, L. J. 1971. Evolutionary significance of leaf architectural features in the 
woody dicots. (Abstract). Am. J. Bot. 58: 469. 


HOPKINS, W. S. 1974. Some spores and pollen from the Christopher Formatigl 4 
(Albian) of Ellef and Amund Ringnes Island, and northwestern Melville Island, | 
Canadian Arctic Archipelago. Geol. Surv, Canada Pap. 73-12. ; 


KEAST, A. 1959. Australian birds: their zoogeography and adaptations to an arid : 
continent. Pp. 89-114. Jn Biogeography and Ecology in Australia. Den Haag: | 
W. Junk. 


MAYR. E. 1972. Continental drift and the history of the Australian bird fauna, ‘| 
Emu 72: 26-28. 


Origin of the angiospermous flora 189 


MULLER, J. 1970. Palynological evidence on early differentiation of angiosperms. 
Biol. Rev. 45: 417-450. 


RAVEN, P. H. & D. I AXELROD. 1974. Angiosperm biogeography and past 
continental movements. Ann. Mo. bot. Gdn 61: 539-673. 


SCHODDE, R. & J. H. CALABY. 1972. The biogeography of the Australo- 
Papuan bird and mammal faunas in relation to Torres Strait. Pp. 257-300. In 
D. Walker (Editor), Bridge and Barrier: The Natural and Cultural History of 
Torres Strait. 


SCHUSTER, R. M. 1972. Continental movements, ““Wallace’s Line’? and Indo- 


malayan-Australasian dispersal of land plants: some eclectic concepts. Bot. 
Rey. 38: 3-86. 


SCOTT, R. A., E. S. BARGHOORN & E. B. LEOPOLD. 1960. How old are 
the angiosperms? Am. J. Sci. 258-A (Bradley Vol.): 284-299. 


P. L. WILLIAMS, L. C. CRAIG, E. S. BARGHOORN, L. J. 
HICKEY, & H. D. MacGINITIE. 1972. “Pre-Cretaceous”’ angiosperms from 
Utah: evidence for Tertiary age of the palm woods and roots. Am. J. Bot. 
59: 886-896. 


SMITH, A. C. 1970. The Pacific as a key to flowering plant history. Univ. Hawaii, 
Harold L. Lyon Arboretum Lecture 1: 1-27. 


1973. Angiosperm evolution and the relationship of the floras of Africa 
and America. Pp. 49-61. Jn B. J. Meggers, A. S. Ayensu, & W. D. Duckworth 
(Editors). Tropical Forest Ecosystems in Africa and South America: A Com- 
parative Review. Smithsonian Inst. Press, Washington, D.C. 


SOLEM, A. 1958. Biogeography of the New Hebrides. Nature 181: 1253-1255. 


—— 1959. Zoogeography of the land and fresh-water Mollusca of the 
New Hebrides. Fieldiana, Zool. 43: 239-359. 


STEBBINS, G. L. 1974. Flowering Plants, Evolution above the Species Level. 
Harvard Univ. Press, Cambridge, Mass. xviii & 399 pp. 


TAKHTAJAN, A. L. 1957. On the origin of the temperate flora of Eurasia. Akad. 
Nauk SSSR 42: 1635-1653. 


————— 1969. Flowering Plants, Origin and Dispersal. Transl. by C. Jeffrey. 
Oliver & Boyd, Edinburgh. 310 pp. 


THORNE, R. F. 1963. Biotic distribution patterns in the tropical Pacific. Pp. 


311-354. In J. L. Gressitt (Editor), Pacific Basin Biogeography, Bishop Museum 
Press, Honolulu. 


———_———— 1968. Synopsis of a putatively phylogenetic classification of the 
flowering plants. Aliso 6 (4): 57-66. 


1969. Floristic relationships between New Caledonia and the Solomon 
Islands. Phil. Trans. R. Soc. Lond. B 255: 595-602. 


1974. A phylogenetic classification of the Annoniflorae. Aliso 8: 
147-209. 


WOLFE, J. A. 1974. Fossil forms of Amentiferae. Brittonia 25: 334-335. 


J. A. DOYLE, & V. M. PAGE. 1976. The bases of angiosperm 
phylogeny: paleobotany. Ann. Mo. bot. Gdn 62: 801-824 (for 1975). 


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On the Origin of the Sycomore Fig 
(Ficus sycomorus L.) in the Middle East 


by 
J, GALIL!, M. STEIN? & A. HOROVITZ? 


Summary 


The distribution area of Ficus sycomorus can be divided into two distinct parts. The 
main area, in which trees produce viable seeds and grow spontaneously follows along the 
Eastern Coast of Africa, from South Africa to Sudan. The northern area, in which no seeds 
are produced and the trees are dependent on man for propagation, includes the Middle 
East and North Africa. In the present paper an attempt is made to elucidate the problem 
of origin of F. sycomorus plants in the northern area. These may be either remnants of 
prehistoric native populations which have lost their ability to set seed or secondary derivatives 
introduced into the area in remote times by man. 


Remnants of fruit bat skeletons in caves from the Natufian period (9.000-7.000 B.C.) are 
taken as a possible indication for the presence of sycomore fig in the Middle East at an 
early date. Remnants of sycomore roots in the upper Nile Valley dating from the Badarian 
period (about 4000 B.C.) also support the assumption of a primary origin of the tree in 
the Middle East. 


It is proposed that, due to loss of the specific pollinator at the dawn of civilization, 
the trees ceased to reproduce spontaneously. Instead they have since been propagated 
vegetatively by man for fruit and wood. 


Introduction 


The sycomore fig Ficus sycomorus L. (Plate la) belongs to the Sudanian 
phytogeographical element. Today this species grows wild mainly in eastern parts of 
Africa, from Sudan and Ethiopia to South Africa (Kruger Park) with extensions 
into Yemen on the Arab Peninsula and into the Namib Desert in Southwest Africa 
(Fig. 1). The trees are most commonly found along stream banks, but also grow 
at other sites where the water table is high, as in the Mombasa area of Kenya. The 
pollinator of the sycomore fig, the wasp Ceratosolen arabicus Mayr (Agaonidae) 
Occurs in these same areas, so that throughout eastern Africa the trees are fertilized 
and produce viable seed. Where conditions are favourable, one finds young plants 
of seed origin. 


Outside its present main distribution area, the sycomore grows in various 
Middle Eastern localities (Rhodes, Cyprus, Lebanon, Israel. Egypt) and in North 
Africa (Libya and Algeria). In these secondary distribution areas (Fig. 1) also, 
the species occurs in wet habitats in the vicinity of streams and springs or in valleys 
and plains where the water table is high. In the Middle East the sycomore does 
not grow spontaneously. The pollinating wasp does not occur here and trees 
produce no seed. 


The two sycophilous wasps which inhabit the syconia in this area, namely 
Sycophaga sycomori L. (Torymidae) and A pocrypta longitarsus Mayr (Torymidae), 
do not carry pollen on their bodies and cannot bring about pollination (Galil and 
Beenowitch, 1968). The present day trees in the Middle East have all been planted 

y man. 


1,3Tel Aviv University, Department of Botany, The Dr. George S. Wise Center for Life 
Sciences, Tel Aviv, Israel. 
2 Kfar Masaryk. 


191 


192 Gardens’ Bulletin, Singapore — XX1X (1976) 


Sycomore figs have been domesticated in the Middle East for their juicy fruits 
which develop in great numbers, for their timber, and as shade trees. A number of 
cultivars can be distinguished which differ in fruit size and shape, in the length 
of the fruit stalk, and, most important, in their ability to produce parthenocarpic 
fruit (Galil, 1968). Two cultivated varieties (Kelabi and Roumi) are known in 
Egypt according to Brown and Walsingham (1917). In Israel the cultivated 
varieties are Belami and Razi. In Cyprus a fifth variety differing from the others 
is grown in addition to Belami. 


The sycomore fig is not the only tropical plant extending into areas bordering 
the Mediterranean. About 100 tropical species of the Sudanian element occur in 
Israel alone (Griinberg-Fertig, 1966). Some of these are prominent trees which 
stand out in their surroundings. Most of these species are confined to the hot, 
sheltered Jordan Rift Valley; others grow in the also relatively warm coastal plain. 
Since these plants reproduce spontaneously and are in their majority of no economic 
value, they must have reached their present Middle-Eastern distribution without the 
aid of man. It is likely that most of them belong to a recent migratory wave which, 
aided by rising temperatures, moved northward from Africa after the end of the 
last glaciation (Galil, 1972). 


Within the Sudanian element in the Middle East, the sycomore fig constitutes 
a special case: first, it has apparently been of special interest to man from early 
times on and second, it is not pollinated and lacks natural means of dispersal in 
its present Middle-Eastern and North-African distribution. In view of the above, 
the present study explores two main alternative questions. Has the sycomore fig 
moved to the Middle East spontaneously as a part of the wild Sudanian element 
and remained in the area after losing its reproductive capacity only because of the 
active help of man, or has man been entirely responsible for its northward trans- 
portation? In the present study these two alternative possibilities are explored. 


Lines of Investigation 


Fossil equivalents of Ficus sycomorus or its close relatives are not available. 
Also a search for palynological evidence is futile since the pollen of the sycomore 
fig remains confined within the syconium and is not dispersed in the air. Accord- 
ingly, the present investigation relies on archaological data only. 


Egypt and later Palestine were important centres of early civilization. The 
organization of State in the Nile Valley, the concept of the immortal God-King, 
the unique cult of the dead and the invention of hieroglyphic writing provided the 
basis for the preservation of evidence on life in ancient Egypt and on the plants 
and animals which accompanied man. Information can be assembled from writings, 
paintings, ornaments, bass reliefs and remnants of dry plant parts found in tombs 
(Laurent-Taeckholm, 1964). Because of the dry desert climate, such plant parts 


are well preserved and can often be identified with certainty. The sycomore fig is - 


richly represented in these records. 


Good sources of information on the sycomore fig in later periods are the Old 
and New Testament and the Talmud (Carmin, 1931; Gali, 1966). While the true 
identity of many Bible plants is controversial, that of the sycomore fig is universally 
accepted. 


In addition to these direct sources of evidence, indirect methods may sometimes 


be helpful. In cases where the plant in question is connected with another organism — 


whose remains are more amenable to preservation, the presence of the plant may 
sometimes be inferred from that of the second organism. Of course such deductions 
can be made only when the two organisms are closely linked. It appears that such 
links exist between the sycomore fig and the Egyptian fruit bat, Rousettus 
aegyptiacus Geoffroy, of which remnants have been found. 


Origin of the sycomore fig 193 


Supposed limit between 
spontaneous and cultivated 
, sycomores 


M2 


mFicus sycomorus,seedless 
e@Ficus sycomorus, spontaneous 


+ Rousettus aegyptiacus 


Fig. 1. Distribution map of seed producing and of seedless sycomore and of the 
Egyptian fruit bat (distribution of bat partly after Harrison, 1964). 


The Sycomore Fig in the Middle East 
in Retrospect 


In Biblical times the sycomore tree was already widespread and well known 
in Palestine (Kings I, Chapter 10: 27; Chronicles II, Chapter 1: 15, Chronicles II, 
Chapter 9: 27). At around 1,000 B.C., King David appointed a curator responsible 
for the sycomores and olive trees in the plain of Lydda (Chronicles I, Chapter 27: 
28). The prophet Amos (Amos, Chapter 7: 14) practiced the ancient method 
of gashing sycomore syconia in the hill area of Palestine. This gashing, by which 
ripening of the syconia is induced at an early stage prior to the emergence of the 
inhabiting wasps, makes the fruit more suitable for consumption (Galil, 1968). In 


the New Testament there is a reference to a tall sycomore tree in Jericho (Luke, 
Chapter 19: 4). 


In ancient Palestine the sycomore tree was held in esteem mainly for its 
timber and less for its juicy fruit or shade yielding crown as was the case in the 
more arid Nile Valley. This is evident from Talmudic literature (100 B.C. to 
400 A.D.), mainly the Mishna and Tosephta, in which many rules governing use 
of the tree and its products are found. 


194 Gardens’ Bulletin, Singapore — XX1X (1976) 


-aenera In his well known book “Enquiry into 
NEW KINGDOM plants”, Theophrastus (372-287 B.C.) also 
gave a detailed account of the sycomore fig 
in Egypt and Cyprus. He described the 

practices. 
. In the dynastic epoch of Egypt (Fig. 2), 
The fruit appears time and again among the 
spree food offerings in burial sites and in necklaces 
ARCHAIC PERIOD 
HISTORIC PER. utensils were made of sycomore wood and 
aaoo « | LATE GERZEAN numerous coffins prepared of sycomore 
EARLY GERZEAN boards have been found in the tombs 
— (Wonig, 1897). 
RES parts and fruits (Lucas, 1948) which can 
be easily identified, are now deposited in 
Archaeological Museum of Cairo contains 
a particularly rich collection of plant parts 
ree Tackholm, 1964). Galil (1967) examined 
a fruit taken from the tomb of Ani of the 


TASIAN 


ISRAEL 


gashing technique and other cultivation 
; the sycomore tree was held in high favour. 
decorating mummies. Many — household 

= 
Well preserved leafy branches, woody 
various museums in Europe and U.S.A. The 
from pharaonic excavations (Laurent- 


NEOLITHIC 


FAIYUM,A' 


JERICHO 
PRE-POTTERY N. 


HELOUAN 
NATUFIAN 


MESOLITHIC MESOLITHIC 


« | {PREHISTORIC PERS 


Fig. 2. Archeological periods in 
the Middle East, beginning with the 
Natufian. 


XXth Dynasty (about 1,100 B.C.). All parts 
of the syconium, including the insects 
inhabiting it, were well preserved and could 
be identified. This syconium is at a late 
developmental stage and the female syco- 
philous wasps had already left it. However, 
the male wasps within the fruit could be 
identified. They are the same parasites which 
inhabit present-day syconia in the Middle 
East. There was no trace of the natural 
pollinator Ceratosolen arabicus, and _ the 
fruit contained no seeds. 


One of the earliest sycomore findings comes 
from Petrie’s excavations in the valley of = 
the Royal Tombs at Abydos (Fig. 3). In his 
report, Petrie (1901) shows a drawing of a or 
dried sycomore fruit, one of the numerous vein 
figs found strung together on threads in the _ ||— Ishango influence 
tomb of Pharaoh Den Setui of the first ee ataue 
dynasty (Fig. 2). Thus we may judge that \. 
throughout the historic period, the sycomore Fig. 3. Prehistoric settlements in 
fig was very popular in Egypt. the Middle Eas 


Origin of the sycomore fig 195 


The earliest archeological records of the plant come from neolithic villages 
and burial sites along the Nile Valley in predynastic Egypt (Fig. 2). These records 
are few and sometimes uncertain. In an account of excavations at Mostagedda 
near Tasa and at Badari on the western bank of the Nile in Middle Egypt, Brunton 
(1937) brings a clear instance of two sycomore fruits found in a tomb of the 
Amratian period at the beginning of the fifth millenium B.C. (Fig. 2). 


The Nile Valley lies 200-300 m below the western desert plateaux and the 
eastern desert which flank it. The seasonal floods and thus the cultivated ground 
do not extend over the entire width of the valley at all points. Between the 
cultivated areas and the eastern and western escarpments there are broad discon- 
tinuous strips of low non-irrigated and non-cultivated desert which are intersected 
by wadis that descend from the plateaux. Under the low present-day rainfall in the 
area (about 25 mm per annum at Cairo) these wadis are now dry. In the low 
desert strips along the valley, large roots leading to remnants of tree trunks have 
been unearthed. Brunton (1937) comments on such roots in Badarian levels of 
the Tasa and Mustagedda excavations, where they were found sometimes adjoining 
the cultivated land and sometimes at a distance from it and always deeply below 
the present desert soil surface. The roots excavated at these levels must have 
predated the Old Kingdom settlements since tombs of this period cut through the 
roots. Brunton concludes from presence of these roots that precipitations in the 
Nile Valley or water supply from the surrounding hills were higher in the fifth 
millenium B.C. than they are today. Similar accounts of roots from the same 
period are brought by Mond and Myers (1937), who also excavated in Middle 
Egypt at Aramant, near Luxor (Plate 1b) of today (Fig. 3). Here the settlements 
were at some distance from the cultivated land along the streams descending from 
the surrounding hills and the roots were found at about 12 m above the flood 
level of the period. Roots from these excavations are shown in Plate 1b. They 
evidently belong to a large tree whose trunk, however, has not been preserved. Sir 
Arthur W. Hill of Kew Gardens who examined these roots reported as follows: 
“The specimen of wood sent for identification appears to be that of Ficus 
sycomorus, although from its indifferent state of preservation, it is not possible to 
identify it with any degree of certainty”. Another sample from the same level was 
identified as a species of Acacia. 


Here too, it has been suggested that the trees belong to the Badarian period at 
the latest. In one of the Badarian cemeteries such roots were found in the rock on 
both sides of a burial chamber which cuts through them. This indicates that the 
trees must have predated the settlement. 


The Fruit Bat as Evidence for Occurrence of Sycomore 
Fig in Natufian Palestine 


The fruits of the various Ficus species, which are juicy and comparatively 
poor in hard matter, are particularly well adapted to consumption by fruit bats. 
Biologists have commented on this link in different parts of the tropics. Williams 
(1928) has shown this in the Philippines and Ratcliffe (1938) in tropical Australia. 
Anderson and Jones (1967) note that the pantropical distribution of the fruit 
eating bats coincides with that of the genus Ficus. Ramirez (1971) notes that fruit 
bats do not occur in New Zealand and Hawaii, which lack native Ficus species. 


One of the bats known to include Ficus sycomorus fruits in its diet is the 
Egyptian fruit bat, Rousettus aegyptiacus (Pteropodidae) (Plate 1c). As seen from 
Fig. 1, the distribution of this large tropical bat coincides roughly with the primary 
distribution of the sycomore fig. The East Mediterranean coast is at the northern 
limits of this distribution. 


196 Gardens’ Bulletin, Singapore — XX1X (1976) 


The fruit bat is active at night and shelters in caves, where it hangs by its legs 
upside down from ceilings, during daytime. Juicy tree fruits and the young shoots 
of various trees constitute its main food. It consumes and swallows soft fruits in 
their entirety; fruits with a hard pericarp or kernels are squashed in the 
mouth and the hard parts spat out. Frequently, the bat carries the fruits to one 
particular branch on a tree and consumes them there. Accumulated dropped seeds, 
and later seedlings, beneath such a point are clear indications for an “‘eating post’. 
Each animal consumes about twice its body weight in fruits or shoots (about 250 g) 
in 24 hours. A daily food supply is necessary and two or three days of starvation 
suffice to kill the animal. 


In Israel the spring to autumn diet comes largely from cultivated fruit trees 
(Fig. 4), causing serious damage to fruit growers. In the cold winter months the 
bats subsist in the area surveyed on fruits of ornamentally grown china berry 
(Melia azedarach L.) and are also observed to nibble pods of the wild-growing 
and cultivated carob, Ceratonia siliqua L., which occasionally remain on the tree 
after ripening in the previous summer. The mandarin (Citrus nobilis Lourt.) 
occasionally serves as another food source during the winter months, In Israel’s 
coastal plain, bats suck the fruits empty of their contents, leaving the hollow peel 


on the trees. Citrus species with thicker peels, such as oranges and grapefruits, are 
not attacked. 


ERIOBOTRYA JAPONICA = 
++ __] 
MORUS NIGRA 


FICUS RELIGIOSA 
FICUS SYCOMORUS 
MELIA AZEDARACH 


MORUS ALBA 
FICUS CARICA 


PHOENIX DACTYLIFERA 


PRUNUS PERSICA 


PSIDIUM GUAJAVA 


PUNICA GRANATUM 


PYRUS COMMUNIS 


CERATONIA SILIQUA 


CITRUS NOBILIS 


Fig. 4. Time table of present-day food plants of the fruit bat. 


While today R. aegyptiacus has a large choice of fruits at its disposal in 
Palestine, this is unlikely to have been the case prior to fruit crop domestication. 
Native East Mediterranean trees and shrubs cannot supply an all-the-year-round 
diet. As far as they have juicy fruits, these ripen in autumn. Young leaves and 
shoots are only available in spring and early summer. 


The sweet fruits of the tropical Ziziphus spina-christi Willd., which abounds 
in the coastal plain and warm valleys of Palestine are not consumed by the bat in 
nature, presumably because of the tree’s thorny stipules. 


Origin of the sycomore fig 197 


As to the locally growing Ficus species, animals in captivity readily consumed 
the fruits of any of the cultivated species offered to them. In the wild state the fruit 
bat frequents the common fig, Ficus carica L. Since this tree bears crops two or 
three times a year, these figs are only available at intervals. This is not the case 
in Ficus sycomorus, which provides a continuous supply of food throughout the 
warmer months from alternately fruiting trees in the same neighbourhood. In the 
coastal plain of Israel trees have been observed bearing up to seven crops a year. 
F. sycomorus can thus bridge over gaps in fruit supply, even under present condi- 
tions. There is only a short fruitless interval during the coldest months of the year. 


On the basis of what has been said, one would expect the bat to show an 
innate preference for F. sycomorus over other fruit trees which are today more 
abundantly available in the area surveyed. This hypothesis was tested in a number 
of experiments. In addition, a test of feeding response to carob was made, since 
the fruits of this local species are available during the cold months of food 
shortage. 


Ten bats were kept in a wire cage which was darkened during daytime. They 
were trained to take their food from plates on a particular shelf. In some cases 
fruits were suspended by threads from the ceiling. The observations, although 
made by electric light, did not markedly interfere with the feeding activities of the 
bats. 


Experiment I (end of November). After sunset three plates were presented. 
One plate contained pieces of guava (Psidium guajava L.) and apple fruit; the 
second contained a mixture of guava and sycomore fruit pieces; the third contained 
only sycomore fruit. After an hour, all sycomore fruit had been consumed whereas 
the apple and guava had not been touched, by themselves or mixed with sycomore 
figs. 

Experiment 2 (end of January). Two plates were presented. One plate con- 
tained a mixture of apples, pears and tomatoes in 12% cane sugar solution; the 
second contained the same mixture with an addition of mashed sycomore fruit 
stalks (not fruits). On the following morning the first plate had remained 
untouched while most of the second plate had been emptied. 


Experiment 3 (end of January). Two plates containing 12% sucrose solution 
were presented to bats which had been starved for three hours in a separate cage. 
To one plate mashed tender sycomore leaves and shoots were added. On con- 
frontation with the food plates the bats immediately approached the plate contain- 
ing leaves and shoots. On the following morning that latter plate was empty while 
the plate containing only cane sugar solution had remained untouched. 


Experiment 4 (February). Eight ripe carob pods were soaked in water and 
suspended in the case at a height of 2 m from the ground. A bowl with drinking 
water was placed on the feeding shelf. Bats that had been kept on half their normal 
rations throughout the preceeding day and had not been fed at all for several hours 
prior to the experiment were released into the cage. After two hours, four of the 
fruits had been nibbled at and broken to pieces. Although the carob pods were 
approached, broken into pieces and even carried to eating posts, they were hardly 
eaten. These pods are too dry to be consumed by the bat and therefore of no 
dietary value. 


The experiments with sycomore fig demonstrate a definite preference for all 
parts of this species over other fruits. The sycomore tree may thus have been an 
indispensible wild food plant which could sustain the fruit bat during the greater 
part of the year in pre-agricultural Palestine. Accordingly, it is difficult to explain 
the presence of the bat in the Middle East of that time without simultaneous 
occurrence of F. sycomorus in the area. It is feasible that the animal’s northward 


198 Gardens’ Bulletin, Singapore — XX1X (1976) 


movement from its primary distribution area in tropical Africa (Fig. 1) has been 
closely linked with the northward migration of F. sycomorus, the fig providing 
sustenance for the bat and the bat serving as an agent of seed dispersal. 


The oldest known pictures of flying foxes are wall paintings found at Beni 
Hasan and date from the twelfth Dynasty, about 2,000 B.C. (Allen, 1939). These 
are of no great help for the elucidation of our problem. But since the bat lives in 
caves, there are good chances for the preservation of its skeleton, which thus can 
serve as indirect evidence for the occurrence of Ficus sycomorus. Fortunately, such 
records are available for a period which predates the earliest archaeological traces 
of the plant, namely from the Natufian level (about 9000-7000 B.C.). 


The Natufian mesolithic civilization is indigenous to an area extending from 
Central Lebanon through Palestine to Helouan in Egypt (Fig. 3). Records of this 
civilization of wide-spectrum food gathering, small game hunting, and fishing have 
been found in different parts of Israel, mostly in caves (Garrod and Bate, 1937) 
but also in open places (Kenyon, 1971). Parts of skeletons of the fruit bats have so 
far been found in two of the caves. Haas (1952) has described R. stekelesi, a 
species very close to the recent form, from the Upper Natufian level of the Abu 
Usba cave, on Mt. Carmel. Also a single molar of R. aegyptiacus was detected in 
the Natufian deposits of the Hayonim cave on the western slopes of the Lower 
Galilee mountains by Bar Yoseph and Chernov (1966). 


It is noteworthy that in earlier Palaeolithic levels in the same caves no 
remnants of the fruit bat have been found. The scarcity of these remnants in the 
Natufian caves, in spite of the favourable conditions for preservations existing 
there, indicates that even in this era the populations of the bat in Palestine were 
very meagre. It is very possible that their establishment was hampered by 
insufficient food supply, especially in the winter. 


Discussion 


The alternatives posed in the introduction, namely whether F. sycomorus 
moved spontaneously to the Middle East with the Sudanian element or whether 
it was brought here by man can now be reviewed. Since there are indications that 
the sycomore fig may have been in the area already in Natufian times, as early as 
the eighth millenium B.C., the primary question is whether man at that time was 
already versed in plant cultivation practices and could transport plants over 
distances. 3 


It is generally accepted that the Middle East and the neighbouring countries 
were the cradle of agriculture in the Old World. Van Zeist (1970), who studied 
the plant findings at Tel Mureybit in the Euphrates Valley, Syria, from the period 
of 8050-7542 B.C., described seeds and fruit of 18 species of wild plants, including 
wild einkorn (Triticum boeoticum Boiss.), wild barley (Hordeum spontaneum 
Koch) and various pulses. At Ali Kosh (Deh Luran plain, Iranian Kurdistan), 
cultivated plant remnants of the period 7500-6750 B.C., including einkorn 
(T. monococcum L.) and emmer (T. diccoccum Schubl.) were found. These area __ 
clear indication of agriculture (according to Renfrew, 1969). The earliest remains _ 
of cultivated plants in the area of Palestine in the prepottery neolithic A level of 
Jericho (about 7000 B.C.) include carbonized seeds of einkorn and emmer, as 
well as various possibly cultivated pulses (Hopf, 1969). It is noteworthy that 
this Neolithic level in Jericho overlies a clear Natufian layer (Kenyon, 1971). j 


As to the beginnings of agriculture in Palestine, Stekelis (1966) regards the _ 
Natufian sickles and mortars as evidence for plant cultivation. Accordingly, he 
puts the beginning of the Neolithicum at about 9000 B.C. and includes the Natufian 
period in it. Yet that culture is generally regarded as mesolithic and pre-agricul- 
tural. According to Kenyon (1971), the Natufian was still a food gatherer, hunter __ 


MAGAD/ 


Wt WoV Vi Vil Vil IX X Xl XM 


1 uw Ww vv vi viv xX xt Xi 


TEMPERATURE 


RAINFALL 


40 SKUKUZA 


iv VW Vi wil ix x Xi xm im Wyvy view viii xX XI MI 


Crp meme) LT 
ey Pty LET PN Bey TT 


RAINFALL RAINFALL 


g ee 
1) PREG 
PUL PSRSeT IIE 


Plate 1. 
Left top: a. Sycomore tree. 


centre: b. Sycomore roots from the Badarian 
period (after Mond and Myers, 
1937). 


bottom: c. Fruit bat. 


Right: d. Climate curves of Cairo (Egypt), 
Magadi (Kenya, East Africa), Lod 
(Israel) and Skukuza (Kruger 
Park, South Africa). 


. 
nT Pk eae - 
Me a4 : 
Sire ete Li 


‘ai ’ - - 
‘ vee Cee * hi a4 
ot) ae wks *\ “7/4 « 9 > 


? 


~ 


Pot are ho ES dg, Gait 


Origin of the sycomore fig 199 


and fisherman and the tools found were used for cutting and pounding wild 
cereals. 


The plant findings of the early Neolithicum in Jericho indicate an advanced 
stage of plant domestication. Arduous and long-continuing processes of selection 
must have preceeded this period. Even if no clear evidence for agriculture in the 
Natufian period is as yet available, probings into plant cultivation must have been 
made in this period. It is feasible that intensive harvesting of wild plants and their 
preparation for consumption with the aid of especially designed tools led even- 
tually to the sowing of these plants near the settlements to ease collection. 
Unfortunately, as long as man did not promote the selection of cultivated plants, 
e.g. non-brittle cereals, no real indication of agriculture can be expected. Further- 
more, Natufian levels have so far not revealed remnants of the wild plants harvested 
and processed with the tools detected in that level. Possibly some of the wild seeds 
found at Tel Mureybit, but whose native habitat at that time was at a considerable 
distance north of the settlement (van Zeist, 1970), were similarly sown by man. 
According to van Loon (1968) some microliths found at Tel Mureybit show 
Natufian influence. 


Another possibility must be taken into account, which is relevant to the 
distribution of the sycomore in the area in ancient times. In addition to seed 
agriculture there are also early traces of dates, grapes and common figs (F. carica) 
in the area, Already in the pre-pottery A Neolithic level of Jericho carbonized 
pips of Ficus cf. carica have been found (Hopf, 1969). Western (1971) reports 
on Ficus charcoals from the same level. It is important te determine finally whether 
these findings belong to the deciduous common fig or to the evergreen sycomore. 
If they belong indeed to F. carica, this species must have been native to Palestine 
and not introduced from South Arabia or Iran as is claimed by Werth (1932) and 
Condit (1937). If, on the other hand, the remnants represent F. sycomorus this 
would be of great help for the elucidation of the problem posed in the present paper. 


The common fig as well as the sycomore can be vegetatively propagated from 
branches stuck into the ground under suitable conditions. This type of plant 
propagation appears to be more simple and easier than seed propagation in which 
the difference between propagule and the grown plant is much greater. There is 
no conclusive evidence as to whether propagation by vegetative parts (vegeculture) 
or seed propagation was the earliest type of plant cultivation in the Middle East 
(Harris, 1969). It must be taken into account that in this region there are several 
suitable habitats for vegetative propagation by branches stuck into the soil. These 
include muddy swamps along the flooded areas of the Nile and sandy soils on a 
high water table along the coastal plain of Palestine, in which branches can 
root readily. 


There are few references as to the domestication of the sycomore fig in 
botanical literature. The German botanist Schweinfurth (1910 p. 34) attempted 
to elucidate the origin of the early Egyptians by tracing the natural distribution 
of two of their sacred trees that were planted in temple gardens, Mimusops 
schimperi Hochst., Sapotaceae and Ficus sycomorus. According to Schweinfurth, 
the two species grow wild in the southwestern hilly parts of the Arab Peninsula 
and in northern Ethiopia, i.e. on the two sides of the Red Sea. Since he found no 
genuinely wild-growing specimens of these species in Egypt, nor in the Upper Nile 
reaches, which support a tropical Sudanian flora today, he concluded that the 
incipient Egyptians brought these alien plants with them from their country of 
Origin in Arabia. While the sycomore fig became well established in its new 
habitats, Mimusops schimperi, the ‘‘Persea’’ of the Greeks, became increasingly 
rare a the Hellenistic-Roman period and almost disappeared in the Islamic 
period. 


200 Gardens’ Bulletin, Singapore — X XIX (1976) 


It appears that Schweinfurth was unaware of the distribution of Ficus 
sycomorus in equatorial and southern East Africa, Also his theories on the origin 
of the Egyptian are questionable. Archaeologists and anthropologists hold that the 
population of the Nile Valley is a heterogenous group of elements part of which 
occupied the Nile Valley already in Paleolithic times and that invasion took place 
not only from the south but also from Libya in the west. Moreover, it is 
unnecessary to evoke migrations of the ancient Egyptians to account for south-to- 
north movements of the sycomore fig. For example, northward migrations of the 
Central African Ishango tribe from Lake Edward in Congo to Khartoum, and 
further north along the Nile Valley are believed to have taken place in the 
Mesolithicum (de Heinzelin, 1962). Here this Central African civilization could have 
come into contact with the southern outpost of the Natufian civilization at Helouan. 


Another proof of possible contacts between the Natufian culture and more 
southern areas is indicated by occurrence of shells of the tropical mussel Cypraea 
moneta in Natufian levels of the Carmel caves in northern Palestine (Garrod and 
Bate, 1937). The northern limit of the natural distribution of this mussel is the 
Gulf of Oman, far to the south. 


Yet the transportation of living plants by man at such remote times is so far 
an open question, Data on the transplantation and shipping of plants appear in the 
archaeological record only relatively late. On the walls of the burial palace of 
Egyptian Queen Hatshepsut (XVIII Dynasty, ca. 1480 B.C.) in Deir el Bahari 
near Thebes, paintings depict a delegation to Punt (Somaliland) loading a vessel 
with living spice plants (Hepper, 1967). Dixon (1969) notes that in all likelihood 
living plants were transported by ancient Egyptians also at much earlier periods. 
However, no definite data are available. 


It appears that in late Pleistocene and early Holocene the climate was humid 
in the Sudan and Ethiopia. Also the present area of the Sahara desert must have 
been more humid at that time and neolithic settlements have been found in areas 
which are most inhabited today. According to Moreau (1963, 1966), the maquis 
of the North African shores extended further south and the Sudanian vegetation 
moved northwards. At least in western North-Africa no desert barrier remained 
between the Mediterranean and Ethiopian territories. Wide desert areas remained 
in the east, but here the Nile Valley with its periodic floods constituted a bridge 
between the Mediterranean and Sudanian vegetations and a south-to-north route 
for the advance of tropical plants. 


Childe (1953) describes the vegetation along the Nile at the last pluvial period 
as follows: ““Today the country south of Cairo is virtually rainless and would be 
utter desert save for the annual irrigation by the Nile flood. But in the pluvial 
period conditions must have been very different. The valleys of the wadis running 
in from the high desert must have been clothed with spring grasses, including quite 
possibly wild cereals and this herbage must have nourished herds of wild asses, 
barbary sheep, urus, antelopes, etc. To find floristic and faunistic environment 
comparable to that encountered by the most ancient Egyptians one must travel 
far upstream into the monsoon zone, On the White Nile the traveller will find, 
growing wild, plants that survived in historical Egypt only in gardens’’. It is likely 
that the sycomore fig which is part of the tropical element in Ethiopia and Sudan 
was among the species growing in the Nile Valley in those times. 


The flourishing vegetation along the Nile described by Childe must have 
become impoverished gradually with the drying of the climate, but even — 


in Badarian times, at the dawn of history, the vegetation was still richer than today _ 


as evidenced by the remnants of large trees and their roots. 


As long as F. sycomorus bore viable seeds, migrating fruit-eating birds and 
bats, especially those which migrate from south to north at the onset of the warm 
season (such as Oriolus oriolus) could have been instrumental in moving the plant 


Origin of the sycomore fig 201 


northwards. When the climate became drier, the flooded areas along the Nile 
became restricted and the sides of the valley bed changed into low desert, the 
tropical vegetation retreated to suitable niches. 


The present absence of the sycomore fig’s natural pollinator in its Middle 
Eastern distribution remains the central question. Did Ceratosolen arabicus 
disappear because of any change in climate? Climates in the Middle East are 
markedly different from the climate of the tropical savannas, the native habitat 
of the sycomore fig. 


Different precipitation regimes or absence of summer rains do not appear to be 
of any significance, since the sycomore occupies humid habitats. Temperature 
differences might be more critical. In the tropical savanna, temperatures are high 
throughout the year and show no diverging seasonal and diurnal extremes (see 
Magadi in Plate 1d). The Mediterranean and desert climates are far less equable. 
In winter temperatures fall below zero (see Cairo and Lod). However, the possibi- 
lity that the Middle Eastern temperature extremes which are withstood by the 
sycomore fig might be too great for its pollinator is ruled out by climatic data from 
Kruger Park in Southwest Africa. Temperature extremes in this park (see Skukuza), 
which occupies southern hemisphere latitudes analogous to those of Middle Egypt. 
are greater than in the Middle East. Yet in the park area the sycomore fig is 
pollinated regularly and sets seed. Young plants of seed origin are observed in the 
park (personal communication from the nature conservator of Kruger Park, 
Mr. P. van Wyk). 


Another possible explanation for the absence of pollinators throughout the 
secondary distribution area of F. sycomorus is loss of compatibility between the 
wasp and new cultivars, resulting from selection and vegetative reproduction for 
many centuries. A clear sign of degeneration in these plants is the production of 
various types of parthenocarpic fruits found in the cultivated varieties (Galil, 1968). 
It is well known that many cultivated plants grown continuously from roots or stems 
lose their fertility and cannot produce seeds any longer. 


To test this point, two attempts have been made to inhabit syconia of F. 
sycomorus in Israel by C. arabicus wasps, brought from Kenya. Both attempts 
failed and no oviposition took place. Yet this is not conclusive evidence for incom- 
patibility of local modern cultivars and the pollinator since in both cases wasps were 
introduced into syconia near the end of the active season of plant and insect under 
local conditions. 


Investigation of the sycomore figs and their sycophilous wasps in Sudan, 
especially at the limit between the wild growing and cultivated trees (Fig. 1) may 
help in the elucidation of the problem. Unfortunately, there is very little information 
on either the tree or its pollinators in this area in the scientific literature. For our 
study, reports on the pollinator Ceratosolen arabicus are more valuable than purely 
botanical information. The dependence of the wasp on the sycomore figs is so 
narrow that in practice the presence of this sole pollinator can be taken as evidence 
for the presence of the tree. 


The most pertinent of the few available data are as follows: Sycophaga syco- 
mori, the specific parasite of F. sycomorus is reported from Nubia (Sudan) on the 
southern bank of the Nile, near Abu Simbel. As already mentioned, this wasp is 
wide spread throughout the whole distribution area of the sycomore fig, including 
Egypt and Palestine, and does not pollinate the flowers. The pollinator C. arabicus 
is not mentioned from that place. 


__ A former Arab resident of Khartoum (Sudan) confirmed that the sycomore 
is extensively cultivated in the surroundings of the city and gashing is practiced 
there for raising the quality of the fruit. Locally the sycomore fruit are called ‘‘those 
of stripped cheeks” after the wide fissures, typical of the ripe fruit sold in the 
market. Thus the sycomore figs growing along the Nile in North Sudan appear to be 
cultivated seedless varieties as in the Middle East. 


202 Gardens’ Bulletin, Singapore — X XIX (1976) 


The pollinator C. arabicus is reported (various authors, including Wiebes, 1968), 
from various parts of Eritrea (Keren, Ghinda) and Ethiopia (Addis Ababa, Caschei, 
Masi). Undoubtedly, the trees growing there are pollinated normally and produce 
seeds. 


In spite of the meagre and incomplete information, the impression of a transi- 
tion between the spontaneous and the cultivated types of F. sycomorus somewhere 
in Sudan is obvious. It appears likely that in desert Moslem northern Sudan, which 
was under Egyptian influence for a long time, the same or similar selected varieties 
of cultivated sycomores are grown as in Egypt. On the other hand, in the woodland 
savannas of southern Sudan, with its negro-nilotic pagan and partially christianized 
population, the tree is still spontaneous. 


Since in desert northern Sudan every piece of irrigated ground on which 
sycomores could survive is in high demand, it is likely that all wild-growing trees 
there were removed by farmers and replaced by useful selected cultivars. Thus a 
more or less sharp boundary between the wild and cultivated types of F. sycomorus 
must have formed, corresponding to the vegetational and ethnic dividing line 
between the northern and southern Sudan. Of course the above hypothesis needs 
verification by detailed surveys of the area. 


Conclusions 


Because of the antiquity of the sycomore in the Middle East, any decision 
between the two alternatives posed in the introduction remains speculative. The 
question is whether the reasonable possibility that in the Natufian period man 
already made the first steps in plant cultivation and propagation from seeds and 
from branches, and the clear evidence of cultural connections between Palestine 
and tropical Africa at those times — provide sufficient ground for assuming that the 
tree was deliberately brought from the south by man. Perhaps the lack of any 
archaeological or geological remnants of the fruit bat in levels below the Natufian, 
i.e. before the onset of agriculture, even in hot and humid periods, supports such a 
supposition. One of the authors of the present paper tends to accept this idea. 


The other two authors believe, together with many prehistorians, that Natufian 
man was not sufficiently advanced for carrying plants along great distances. The 
presence of the sycophilous parasite Sycophaga sycomori within the figs throughout 
the Middle East indicates that the movement of the trees from south to north must 
have taken place step by step. 


The follow-up of the changes of climate and movement of vegetation during 
late Pleistocene and early Holocene provides a sufficient basis for the conclusion that 
the sycomore fig could have reached its secondary distribution area together with 
other components of the last migration wave and that it started its existence in the 
Middle East as a spontaneous, wild-growing plant. Only afterwards, perhaps at the 
early Neolithicum or even later when man started to cultivate plants and select — 
them, cultivars were developed which lacked their compatibility with the pollinator _ 
and consequently lost their ability to produce viable seeds. | 


The clear dividing line between wild growing and cultivated sycomores in Sudan 
is due to man’s interference and is in fact an ethnic and cultural boundary. 


Evidence for the presence of F. sycomorus in the Middle East in ancient times | 
is far from satisfactory, especially since the data supporting the presence of the plant | 
in Natufian Palestine are based on an indirect method of enquiry. But all possible | 
sources of information have not been exhausted. The only fig from Pharaonic tombs | 
which was searched for the presence of pollinators and seeds belongs to a compara- | 
tively recent period (XX Dynasty, about 1100 B.C.). It appears that the sycomore | 
of that time was already identical with the recent form. Studies of additional figs | 
from earlier dynasties should provide critical information. 


Origin of the sycomore fig 203 


The identity of Ficus pips and charcoals found at the pre-pottery Neolithic layer 
of Jericho with either F. carica or F. sycomorus should be established. Soil samples 
and coproliths from Natufian caves should be searched for presence of F. sycomorus 
seeds. Seed findings from earlier periods could provide the basis for a more definite 
decision as to the origin of the sycomore fig in the Middle East. 


Acknowledgments 


The authors are indebted to Prof. E. J. H. Corner (Cambridge), Mr. N. Hepper 
(Kew) and Mr. J. Roth (Shaar Agolan, Israel) who have kindly read the manuscript 
and offered many helpful suggestions; thanks are also due to Mr. S. Shaeffer for the 
illustrations and Mr. A. Shuw for the photographic work. 


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Origin of the sycomore fig 205 
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A Short History of Fig Wasp Research 
by 
J. T. WIEBES 


Department of Systematic Zoology and Evolutionary Biology 
University of Leiden, The Netherlands 


For convenience, the history of fig wasp research may be divided into four 
periods. Mayer’s “‘Zur Naturgeschichte der Feigeninsecten’’ (1882) appears to 
present the first natural break. On the one hand, in giving a comprehensive review 
of older literature, it is the conclusion of its period. On the other hand, in being 
one of a number of contemporaneous reports on exotic fig wasps and, above all 
things, as a precursor to Mayr’s paper of 1885, it also is the opening of a new era. 
In a way, Grandi’s revision of the Agaonidae described by Mayr, and its accessory 
world catalogue (1928d), would form a similar stage half a century later. Between 
the two, past the times that scientists merely looked all wonder at figs and their 
wasps, we find the period in which the warp of fig wasp taxonomy was stretched. 
Some of the weft, it is true, was of very inequal capacity. 


After 1928 we find more than a quarter-century of miscellaneous reports, waifs 
and strays in comparison with Grandi’s synthesis. Then, in the fifties, a new activity 
arises with a gradual shift of interest to the symbiosis of figs and wasps, its 
mechanism and evolution. 


In the present review I shall not confine myself to data on the Agaonidae. In 
the survey of our knowledge of fig wasp biology, we cannot dispense with their 
Torymid mess-mates. An outline of their nomenclatorial history is included in the 
first chapters. For data on pre-Linnean literature, and for a more complete 
discussion of eighteenth-century papers, I here refer to Mayer’s review of 1882: 
their biological significance is negligible. 


Wonder (the period before Mayer, 1882) 


In the “Systema Naturae’’, Linnaeus named two fig insects viz., Cynips psenes 
from oriental Ficus carica and C. sycomori from the sycomore fig of Egypt. These 
insects were generally misidentified until a hundred years later largely, it would 
seem, because of the confusion created by Linnaeus himself. 


Linnaeus’ pupil Hasselquist (1757), in his itinerary of a voyage to Palestine, 
described Cynips ficus and C. caricae from Ficus carica, and C. cycomori from 
F. sycomorus (see table 1 for a concise survey of the nomenclatorial history). These 
descriptions, with only a few small alterations, were repeated in the second part 
added to the German translation of the “‘Iter’’ (1762). In the meantime Linnaeus, 
presumably having decided that Cynips ficus and C. caricae probably were the two 
sexes of one species, united them under the name Cynips psenes. The original 
description of C. ficus ‘‘corpus totum rufum”’ and thus, implicitly, the description 
of C. psenes, did not seem to fit the shiny black insect Gravenhorst (1829) described 
as Blastophaga grossorum: the nomenclatorial outcome of a pronounced sexual 
dimorphism. 


207 


208 Gardens’ Bulletin, Singapore — XX1X (1976) 


Linnaeus (1758) redescribed Cynips sycomori and unfortunately added a 
character of the Agaonidae ‘“‘antennae ... basi crasso-conicae”’. This, and the 
inadequate labels of the specimens in the Linnean Cabinet (Saunders in Waterhouse, 
1881), led Westwood (1840) to the description of Blastophaga sycomori, which 
soon proved to be identical with C. psenes (see Loew, 1843). Genuine C. sycomori 
was renamed Sycophaga crassipes Westwood (1840) although Forskal, as early as 
1775, knew both sexes of what he rightly named Cynips sycomori. 


There remain Cynips caricae, and Ichneumon ficarius Cavolini, 1782. Loew 
(1843), ‘“‘auf Linné’s Autoritat’’, accepted the identity of Cynips ficus and C. caricae, 
but according to Waterhouse (1881) the two must certainly be considered distinct 
species. Confusion was complete when Saunders (1883a: 20) listed three species of 


Blastophaga viz., 
sp.l1. B. ficus, Hasselq.; C. psenes, Linn.; B. sycomori, Westw. 
sp.2. B. caricae, Hasselq.; C. psenes, Linn. 
sp.3. B. grossorum, Grav. 


Half a year later, Saunders (1883c) alluded Cynips caricae to Idarnella West- 
wood (Jdarnodes Westwood, both names of 1883: a, and c, respectively) for which, 
however, Philotrypesis Forster (1878) proved to be an older name. Except for 
Mayer, 1882 (and later, myself: Wiebes in China, 1962) no one seems to have 
recommended the use of the specific epithet ficarius as used by Cavolini, 1782. In 
a way, Westwood (1883c: vii) did, but he regarded ficarius distinct from caricae. 


Table 1. Survey of the nomenclatorial history of Blastophaga psenes, Philotrypesis 


caricae and Sycophaga sycomori. 
Blastophaga psenes (Linnaeus, |Philotrypests caricae Sycophaga sycomort 
1758) |(Linn. in Hass., 1762) |(Linnaeus, 1758) 
Cyntps eycomort 


Cyntps ficus 

Cyntips sycomort’ 
Cynips sycomort 
Cyntps sycomort 


Cyntps caricae 
Cyntps psenes 
Cyntps ficus Cynips caricae 


Linn. in Hasse, 1757 
Linnaeus, 1758 

Linn. in Hass., 1762 
Forskal, 1775 
Cavolini, 1782 
Gallesio, 1820 
Gravenhorst, 1829 
Westwood, 1840 
Loew, 1843 
Forster, 1878 
Saunders, 1878 
Waterhouse, 1881 
Westwood, 1882 
Mayer, 1882 
Saunders, 18834 
Saunders, 1883¢ 


Westwood, 1883c 


Ichneumon psenes| Ichneumon ficarius 
Chalets psenes |Chalcts centrinus 


Blast. grossorum 


Sycophaga crasstpes 
Sycophaga sycomort 


Blast. sycomort 
Blast. psenes 
Philotrypests Longtcauda 


Sycophaga crasstpes| 
Sycophaga sycomort 
Sycophaga crasstpes 
Sycophaga sycomort 
Sycophaga crasstpes 


Blast. grossorum|Blast.psenes 
Blast. grossorum| Blast. ficus [Cyntpe caricae] 
psenes 


Blast. grossorun Iehneumon ficartus 
Blast. grossorum| Blast. ficus Blast.caricae 
Idarnetla caricae 
Idarnodes caricae 
eg ficarius 
Philotrypests caricae 


Mayr, 1885 


It took two recent decisions (1964, Opinion 694; 1974, Opinion 1018) to validat | 
Philotrypesis caricae (Linnaeus in Hasselquist, 1762) as the name of the common ~ 
inquiline of Ficus carica, in the same sense as it had been used by Mayr (1885), 


Fig wasp research 209 


Grandi (1921b, 1930) and Joseph (1958). In the opinion of 1964, Blastophaga 
psenes (Linnaeus, 1758) was validated as the name for the pollinating insect. 


Dalman (1818) expressed his wonder in the name of the fig insect he described 
from Sierra Leone: Agaon paradoxum. Agaon was taken as the basis of the family 
name by Walker (1846), after Westwood recognized the affinities of Agaon and 
Blastophaga and, like Latreille (1825), classified them with the Chalcididae. Billberg 
(1820) as well as later Schulz (1906) emended Agaon to Agaum; Kieffer (1911) 
would create a synonym Courtella (see Wiebes, 1968b). 


It is unfortunate that the specimens recorded by Coquerel (1855) from La 
Réunion cannot now be found, and are probably lost. Three out of four of his 
species from Ficus terragena (probably, the same as F. mauritiana Lam.) are types 
of generic names viz., Sycocrypta with S. coeca, suppressed in Opinion 682 (1963) 
for Ceratosolen Mayr, 1885; Apocrypta with its type A. perplexa, and with A. 
paradoxum which belongs to Sycophaga Westwood, 1840; and Chalcis explorator, 
which was taken by Ashmead (1904a) as the type of Apocryptophagus: most pro- 
bably it is one of the Sycoryctini, and not Jdarnes as Walker (1871b: 60) suggested, 
nor Sycophaga as Westwood (1883b: 379) had it. 


Motschulsky’s (1863) material I have seen in the Moscow Natural History 
Museum. Platyscapa frontalis belongs to Waterstoniella Grandi, 1921a; Platyneura 
testacea most probably is a species of Parakoebelea Joseph, 1957a. Validation of 
the older names would create nomenclatorial changes in the Agaonidae and 
Torymidae. 

From the West Indies Walker (1843) described Idarnes carme, which seems 
to be the same as Tetragonaspis Mayr, 1885 (as Mayr supposed but could not 
decide from Walker’s description). This leaves the Old World species of “‘Jdarnes’’ 
without a generic name (see Wiebes, 1966a: 155-156; 1968a: 310-311), but see 
the suggestion by Gordh (1975: 439) that Jdarnomorpha Girault (1915b) could 
serve. Compare, however, also Hill (1967d: 94), who listed Idarnomorpha as a 
synonym of Ofitesella Westwood! The type of J. carme is a female specimen in the 
British Museum (Natural History), from which the head was already lost when 
Westwood (1883a: 37, note) studied it; now it seems to be completely lost, and a 
neotype had to be designated (Gordh, 1975: 426-427). In the same 1843 paper 
Walker described Paphagus (Walker, 1871b: 65, ““Paphagus Sidero ... belongs to 
the Agaonidae”’), which was also by Mayr (1885: 151) mentioned as if he supposed 
it to be a fig wasp. Ashmead (1904a: 319, 499) cited it as one of the Pteromalidae. 
More confusion was created by Walker’s description of wasps destructive to the 
fig in India, originally in 1871 (b), and again (posthumously) with different names 
in 1875 (see Patton, 1884; Wiebes, 1967e: 400-402). 


In all, by the time Mayer wrote his review, there were known eighteen fig wasps, 
be they under twenty-four names. Most of these were known in one sex only, but 
they represented a fair sample of all but one of the larger groups now recognized 
(see table 2). Their host figs, as far as then known, belong to Urostigma (Ficus 
benghalensis from India), Ficus (F. carica), and Sycomorus (F. sycomorus from 
Egypt, and F. mauritiana from La Réunion). 


Although Linnaeus (Hegardt, 1749) already explained the process of caprifica- 
tion by supposing that the insects brought the farina from the wild fig, which con- 
tained male flowers, to the domestic fig, which contained only female flowers (see 
Westwood, 1840: 215), several authors doubted or opposed this explanation. Mayet 
(1882, partly basing himself on Solms, 1882) extensively dwelled on this point. 
Most of his views on Ficus carica were corroborated by data from Grandi (1920a, 
1929a), Buscalioni & Grandi (1936, 1938), and Joseph (1958), and will be discussed 
in a later chapter. 


210 Gardens’ Bulletin, Singapore — XX1X (1976) 


Table 2. Fig wasps known in 1882. 


-see table 1- Blastophaga psenes (L., 1758) Joseph, 1958: 201 
Agaon paradoxum Dalman, 1818 Agaon paradoxum Dalman Wiebes, 1968b: 346 
Syeocrypta coeca Coquerel, 1855 Ceratosolen coecus (Coquerel) Opinion 682, 1963 
Platyscapa frontalts Motschulsky, 1863| Waterstontella frontalis (Motsch.) | (new comb.) 


TORYMIDAE, Sycophaginae 
-see table 1- Sycophaga sycomort (L., 1758) Wiebes, 1968a: 311 
Idarnes carmée Walker, 1843 Idarnes carme Walker Gordh, 1975: 425 
Apoerypta paradoxa Coqe, 1855 Sycophaga paradoxa (Coquerel) Westwood, 1883b: 379 
Platyneura testacea Motschulsky, 1863 | Parakoebelea testacea (Motsch.) (new comb.) 


Apoerypta perplexa Coquerel, 1855 Apoerypta perplexa Coquerel Westwood, 1883b: 379 


Chalets exploratory Coquerel, 1855 Apoeryptophagus explorator (Cog.) | Ashmead, 1904a: 238 
Idarnes stabtlis Walker, 1871 } Sycoscapter stabilis (Walker) Wiebes, 1967e: 407 
Idarnes orientalis Walker, 1875 
esee table i- | Philotrypests caricae (L. in Hass.)| Joseph, 1958: 201 

Idarnes transtens Welker, 1871 } Philotrypests transtens (Walker) Opinion 1018, 197% 
Polanisa lutea Walker, 1875 

Sycobia bethylotdes Walker, 1871, ¥ | Walkeretla temeraria Westwood Wiebes, 1967e: 402 
Idarnes pteromalotdes Walker, 1871 


} Micranisa pteromalotdes (Walker) Wiebes, 1967e: 40% 
Micranisa Walker, 1875 


TORYMIDAE, Epichrysomallinae | 


Sycobta bethyloides Walker, 1871 } Sycobta bethylotdes Walker Joseph, 1957a: 128 
Agrtanisa myrmecoides Walker, 1875 

EURYTOMIDAE, Eudecatominae | 
Sycophila megastigmotdes Walker, 1871 } Sycophila megastigmotdes Walker Burks, 1969: 119 
Pséudtsa smtcroides Walker, 1875 
Sycophila decatomoitdes Walker, 1871 } 


Sycophila decatomotdes Walker Burks, 1969: 119 
Isantsa deeatomotdes Walker, 1875 


Warp and Woof (from Mayer, 1882 to Grandi, 1928d) 


Before 1882 only a few shipments of tropical or subtropical fig insects were 
sent to Europe. Then, in 1882, Mayer reported on the collections made by Solms, 
that is, taken from figs in European herbaria or collected in Java, or brought from 
Egypt by Schweinfurth and Valentiner; moreover, Fritz von Miiller (1886-1887) | 
sent several samples from Brazil. Thus began the stream of shipments to Europe, | 
and to America, where research was soon to start. } 


I shall now discuss some works of more general importance viz., those by Mayr 
(1885), Ashmead (1904a) and Grandi (1916-1917). Table 3 contains the classifica- 
tion of most of the genera discussed below; a more complete list of the Syco- 
phaginae was presented by Hill (1967d: 92-96). 4 


Mayr distinguished between three categories of fig insects viz., gall makers — 
(according to Mayr: probably all ‘‘Agaoninen’’, certainly those of the genus — 
Blastophaga), Hymenoptera parasitic upon larvae and pupae of the gall makers, and — 
visitors (““Feigenbesucher’’) such as ants and fruit flies. Next to several genera of 


Fig wasp research 21] 


the modern family Agaonidae, the first group also contained Crossogaster and 
Sycophaga (inclusive of Apocrypta!). It is now known (Galil, Dulberger & Rosen, 
1970) that at least Sycophaga sycomori does cause “‘gall-tissue”’ in Ficus sycomorus. 
It was mainly the female morphology (the facial groove and other characters related 
to the way of entering the fig receptable) that characterized the Agaoninae in 
Mayr’s restricted sense (with Walker, the Agaonidae contained all fig wasps). 
Undoubtedly, Mayr classified his Agaoninae with the Chalcididae. In 1906, Mayr 
added new records and descriptions. 


Table 3. Fig wasp classifications by Saunders, Mayr, Ashmead and Grandi compared. 


SYCOPHAGIDES 
Prionostomata ') "Agaoninen" AGAONIDAE AGAONINAB 
Agaoninae Agaonini AGAONIDAB 
Agaoninae 
Agaon Agaon Agaon Agaon Agaon 
Alfonstetla Alfonstetla 
Allotrtozoon Allotriozoon 
Eltsabethtella Eltsabethietla 
Pletstodontes Pletstodontes | Pletstodontes| Pletstodontes Pletstodontes 
Tetrapus Tetrapus Tetrapus Tetrapus 
Blastophaginse 
Fupristina Euprtstina Eupristina Eupristina Eupristina 
eyeberypts li Ceratosoten 
Ceratosolen Ceratosoten Ceratosoten. 
Kradibta } Blastophaga Blastophaga Blast. $.Str. | Blastéphaga s.1. 
‘Blastophaga Risenta { Secundetsenta | 
Paqogeayns Pegoscopus ©) 
Jultanella 
Valentinettla 
Ltvorrhopatum Ltporrhopatun 
Sycophaginae | 
Platyscapa Platyscapa 
. Waterstontetla i Waterstontelta 
TORYMIDAB 
Sycophaginae 
Haplostomata by Sycophagini 3) 
Crossogaster Crossogaster Crossogaster Crossogaster 
Sycophaga 
apearyptc Sycophaga Sycophaga Eycophaga Sycophaga 
paradoxa 
perplera . Apocrypta Apoerypta 
Me TORYMIDAE "TORYMIDAE teocrypte 
Idarninae Idarnini 
Gontqagaster Gontogaster Gontogaster 
SYCOLACIDES 
Idarnes etc. Idarnes etc. Idarnes etc. Idarnes ete. Idarnee etc. 


1These names are emendations of Prionastomata and Aploastomata, respectively (Saunders, 
1883b). 

2 Hill (1967d: 91), following Waterston (1920a), gave preference to Secundeisenia Schulz (1906) 
over Pegoscapus Cameron (1906). According to Ramirez (1970a: 11), the date of publica- 
tion of Cameron’s paper is June Ist, while Schulz (1906: 356) cited Eiseniella Ashmead 
(July 13th, 1906), showing that Secundeisenia postdates Pegoscapus. 


3 Various genera, now classified with Otitesellini and Sycoecini, omitted. 


212 Gardens’ Bulletin, Singapore — XX1X (1976) 


It may be noted that Saunders, as late as 1883 (a: 11-20; b: v—vi), when he 
divided Walker’s Agaonidae into phytophagous ‘‘Sycophagides”’, and other, pre- 
sumably parasitic types, classified the former with the Cynipidae. The latter, con- 
sidered to have “‘no tribal affinity with Agaon’’, were named “‘Sycolacides’’. West- 
wood, in 1882 as in 1840, allocated Agaon to the Chalcididae. The Haplostomata 
of Saunders, being the group that might prove to be parasitic, were excluded from 
the Agaonidae by Patton (1884: xvi): “‘should they prove to be sycophagous the 
term Sycophagides should be retained for them, as the genus Sycophaga is included: 
otherwise Saunders’ term Sycolacides may be employed”’. 


Ashmead (1904a) classified Agaon etc. in the nominate subfamily of the 
Agaonidae; Saunders’ Haplostomata, and also Platyscapa and Crossogaster, formed 
the subfamily Sycophaginae. Most of the parasitic types were classified in the 
Torymid subfamily Idarninae; some others in Monodontomerinae (Physothorax, 
Plesiostigma; compare a recent paper by Burks, 1969) or in Miscogasteridae 
(Aepocerus; see Mayr, 1906: 180-181). Ashmead’s treatment of the Chalcidoidea 
set the stage for a long time to come; Schmiedeknecht (1909) duplicated this classi- 
fication in his volume of the ‘‘Genera Insectorum’’, but considered the Chalcid 
flies a family instead of a superfamily. In this, Grandi at first followed Schmiede- 
knecht. 


While the fig wasps formed only a small part of the amount treated by 
Ashmead, Grandi (from 1916 onwards) in an impressive series of major publica- 
tions, specialized on these smaller groups. He described many species and genera 
from Africa (1916a, 1917b), Australia (1916b), Ceylon and India (1916c), Java 
(1917a), the Americas (1919), etc. In so doing, or in separate publications, he pro- 
vided morphological descriptions of Blastophaga (1920a) and Tetrapus (1925a), 
now classified in two subfamilies of the Agaonidae; of Sycophaga, Apocrypta 
(males only) and Crossogaster (1916a), Philotrypesis (1921b), and Otitesella (1922b) 
— examples of five out of the six tribes now recognized in Sycophagine Tory- 
midae — and Neosycophila (1923d), a genus of the subfamily Epichrysomallinae. 
Thus, except for the tribe Sycoryctini and the subfamilies Toryminae and Eudeca- 
tominae, all major types were dealt with! In 1928 (d), Grandi revised the Agaonidae 
from Mayr’s collection, and he published a world catalogue of the group. 


In Grandi’s opinion, Sycophaga, A pocrypta 
and Crossogaster formed the Agaonine tribe 
Sycophagini (i.e., Saunders’ Haplostomata), 


Table 4. Classification of fig wasps. 


: 2 Agaonidae 
while the other parasites were part of npuitlens 
Ashmead’s subfamily Idarninae of the Tory- misichonsialial 
midae (with Goniogaster Mayr, the female of Seaniittin 
Apocrypta; see, however, Grandi, 1923d: 113, Toryainas Ko.ghpditqeetionias 
note). Among the Idarninae, Grandi (e.g., Pee é 
1925b) distinguished between the “TIdarnini Grodauaal 
veri” and two biological groups containing cantina 
Otitesella and related genera, and Neosyco- groaeveeiel 
phila. Much later (1952a, 1955b), he would Pailotespedied 
again note on these groups, and in 1963 (c) PP hater 
he considered my proposition (Wiebes, 1961b) man re 
to include the Sycophaginae with the Idarninae. Epichrysomallinae 
Anticipating a later discussion of the recent Eurytomiade 
classification of fig wasps, I here include table Eudecatominae (e.g., Sycophila) 


4 to provide a synopsis of the larger groups. 


Grandi was particularly interested in the morphological adaptations of insects 
to special conditions. The various groups of fig wasps and their adaptations were 


Fig wasp research 213 


to be compared with the modifications in groups such as mining insect larvae. The 
Neosycophila-wasps, developing in rather superficial galls from which the mature 
females and males escape directly to the outside, were considered to possess no 
adaptive deviations from a normal Chalcid morphology. The females of Otitesella 
and related genera too, were considered rather normal. Their males, however, and 
those of most other groups now classified with the Sycophaginae (Sycoecini 
excepted), are apterous and also otherwise rather aberrant. The females of most 
Sycophaginae (not the Otitesellini and Sycoecini) have long ovipositors and in many 
instances the gaster can be lengthened by telescoping the segments, or the one or 
two last segments are tubularly lengthened (these characters would later serve as 
differential characters of several tribes). 


The females of the Agaonidae are characterized by the depression of the head; 
the presence of a facial groove; the reduction of the mouth-parts, although special 
mandibular appendages are developed; the modification of the proximal antennal 
segments; the armature of the fore and hind tibiae. (Grandi did not know the func- 
tion of the pollen pockets.) The males have atrophied mouth-parts; no ocelli; 
reduced antennae situated in grooves; no wings; etc. Some of these characters were 
also found with some Ofitesella-like females (i.e., the modern Sycoecini; not our 
Otitesellini!) and, in the male sex, also with the “Idarnini veri’: Grandi rightly 
considered these attributes correlated with the way of entering the fig receptacle 
(females), or with the life within the receptacle (males). For these modifications, 
which were on several occasions profusely discussed and illustrated (Grandi, 1923a, 
1925b, 1929c, 1936c, 1958a, 1959, 1961b), Grandi suggested several ways of origin 
viz., involutions, rudimentations or disappearance of (parts of) organs, or hypertelic 
development, displacement, and transformation, and also the development of new 
(parts of) organs. Some, although always connected with the function the organs 
have to perform “generally do not seem to be necessary, often not even useful, 
sometimes even a hindrance (if not disgenic)”” (Grandi, 1959: 223). What Grandi 
seemed to imply is that not all modifications were of apparent importance to the 
individual or specific existence of the bearer: “e quindi, apparentemente, non 
vantaggiose alla specie’? (1925b: 311). To understand much better, however, the 
pros and cons of any particular modification (or rather, its function in the composite 
syndrome in which several modifications coincide), much more would have to be 
known of the behaviour of the wasps in symbiosis. 


Before mention will be made of Grandi’s important observations on Blasto- 
phaga psenes and Philotrypesis caricae, which will be the main theme of the next 
chapter, I shall now discuss the papers by Froggatt (1901) and Pemberton (1921) 
on Australian Pleistodontes froggatti, and by Baker (1913) and Williams (1928) 
on some Philippine wasps. Actually, Froggatt’s paper was not the first on the 
biology of insects living in figs, and he could refer to several papers on caprification 
e.g., by Cunningham (1889) on the fertilization of Ficus roxburghii (F. auriculata 
Lour.), Howard (1899) and Eisen (1891) on attempts to introduce Blastophaga 
psenes into California as a pollinator for Ficus carica. Cunningham described the 
flowers of F. auriculata, and the effects of the presence of insects upon them: he 
concluded that it is not pollination that causes development, but the irritation 
following the act of oviposition. The same observation was made by Treub (1902) 
for Ficus hirta of Java, although here some germination of pollen grains was 
observed. In California, some of the fig growers considered the process of caprifica- 
tion of no practical value, but only the survival of an ancient custom blindly handed 
down from father to son in Mediterranean regions. Yet, in many places the wasps 
were successfully introduced (see table 5; Ramirez, 1970b, table 2 listed figs 
introduced in absence of Agaonidae: they did not set seed). 


214 Gardens’ Bulletin, Singapore — XX1X (1976) 


Table 5. Fig wasps introduced with their hosts. 


- 
e] 


& Asia ty Blast. psenes 2 Phoenicians Mediterranean | 2 1100 B.C. 


+ | Eisen, 1901: 16-26 
Blast. psenes H.E. Van Deman California 1890 = | Swingle, 1908: 181 
Blast. psenes James Shim California 1891 (twice)| = | Swingle, 1908: 181 
F. cavica Blast. psenes | Thomas Hall California 1892 ~ | Swingle, 1908: 181 
FP. carica "Asia Minor"| Blast. peenes A.C. Denotovitch | California 1895 = | Swingle, 1908: 181 
P, cartea Naples Blast. psenes | W.T. Swingle California 1898 - | Swingle, 1899: [8], 1908: 181 
-P, cavica Algeria Blast. peenes | W.T. Swingle California 1899 + | Swingle, 1899: [8], 1908: 181 
P. carica 2 Blast. psenes 2 Australia 2 + | Robson, 1911; Savage, 192% 
F. cavica ? Blast. psenes 2 Pretoria 2 + | Waterston, 1920a: 128 
| F. macrophytia| Australia P. froggattt F.M. [uir] Hawaii 1921° + | Muir, 1922: 12; Wiebes, 1963b: 307 
FP, vubiginosa | Australia P. tmpertalis 2 Hawaii 1922 + | Timberlake, 1923: 200 
FP. alba 2 [Blastophaga] [Fosberg] Hawaii cas 1930 + | Corner, 1958: 18 
P. fistulosa 2 [Ceratosolen] [Fosberg] Hawaii cae 1930 + | Corner, 1958: 18 
FP. veligioea | East Asia B. quadraticeps 2 Israel ? + | Galil & Eisikowitch, 1968e: 356 


1 The observation that the entomofauna of the sycones of Ficus carica is more complete in 
India than elsewhere (i.e., it harbours there a species of Sycoscapteridea not found in Europe, 
Mayr, 1885: 153; Joseph, 1957a: 119), adds to the probability of Asia being its homeland. 


Ficus macrophylla, the fig observed by Froggatt and Pemberton, is different 
from the edible fig in that it is monoecious, bearing male, female and gall flowers in 
one syconium (fig. 2). In other species, male and female flowers occur in separate 
figs e.g., in Ficus carica and F. nota (studied by Baker and Williams) (fig. 1; 
dioecious figs). The entrance of the female Pleistodontes wasps through the narrow 
ostiole of Ficus macrophylla was described by Pemberton (1921) as a forward-reach- 
ing movement to fix the tips of the hook-like mandibles into the tissue in front and 
then, in lowering them, to draw the whole body forward over a short distance. The 
saw-like serrations of the mandibular appendage prevent the head from slipping 
back. Usually up to five or six wasps will successfully enter a single receptacle, and 
immediately begin egg-laying. The larva hatching from the egg, matures and 
pupates within the gall-flower. The wing-less males hatch first out of their galls, 
and they start in search for a gall containing a female; they fertilize the females by 
inserting the tip of the abdomen through a hole gnawed in the galls. The females 
leave the fig by boring a hole through the wall of the receptacle at any point. In 
doing so they become covered with pollen from the ruptured male flowers which, 
unlike in many other species of Ficus where they are concentrated around the 
ostiole, are not confined to any particular part of the fig. ‘““Much of this pollen 
must be brushed from the wasp’s body during the short but strenuous trip — 
to the young fig — , yet sufficient is carried over to secure ample pollination for 
a great many female flowers” (Pemberton, 1921: 306): it was not noted how the 
pollen is being transported, and this would remain unknown until 1969! 


Many of the details described for Pleistodontes froggatti were identically 
observed for Ceratosolen notus and the dioecious Ficus nota (see Baker, 1913), and 
for Blastophaga psenes and Ficus carica (the former, however, does possess pollen 
pockets, just as does P. froggatti, but these are completely lacking in the latter). 
Important differences are found in the place where the females leave the receptacle, — 
which is through the ostiole in Ficus carica and F. nota (where it is often enlarged — 
by the males). Williams (1928: 11-13) listed a number of instances of males — 
enlarging the ostiole or tunnelling close to it. Later we shall learn how important . 
this kind of male behaviour can be. 


» 
a: 
. 


Fig wasp research 215 


~ 


Sycophaga 


aS 


Figs. 1 & 2. Cycles of dioecious (Ficus carica, fig. 1) and monoecious figs (F. sycomorus, 
fig. 2), and their wasps (Blastophaga indicated in fig. 1; three with names added in fig. 2). 
The letters correspond with those used in the text (p. 220); a, o'; 5, short-styled, and c, 


long-styled Q flowers. Adapted from Wiebes (1965a) and Galil & Eisikowitch (1968a). 


216 Gardens’ Bulletin, Singapore — XX1IX (1976) 


In comparison with 1882, by 1928 the number of known fig wasps was greatly 
augmented. For a paper by Van der Vecht (1973), I once computed these numbers 
of the Agaonidae: they were depicted in a graph reproduced here (fig. 3). 


Waits and Strays (thirty years 
of miscellaneous reports) 


The period between 1928 and 
1958 is characterized by a number 
of small papers on fig wasps from 
all parts of the world. As such, it 
forms a continuation of the series 
already begun by Grandi, Waterston 
(1914-1921, mainly on new African 
and some Indo-Malayan forms), 
etc. Special mention should be 
made of Grandi’s important con- 
tributions to the knowledge of the 
fauna of South America (1934, 
1936b, 1938a; see also Hoffmeyer, 

: 1932; Mangabeiro Filho, 1937; 
1800 1850 1900 1950 Blanchard, 1944) and of Ishii’s 
Fig. 3. Trend curve for the number of descriptions of Japanese parasites 


known Agaonid species. From Van der Vecht (1934). Also some of the papers 
(1973). by Girault (1913-1939) fall into this 


period, and they certainly may be 
named waifs and strays (see De Santis, 1961)! Between 1951 and 1957, Risbec 
published a number of papers on African and Malagasy Chalcidoidea; see Wiebes 
(1970a) for a revision of the fig wasps. Joseph started his series of papers on Indian 
fig wasps in 1952; it was concluded later in cooperation with Abdurahiman. 


As mentioned in the previous chapter, Grandi contributed an important mono- 
graph on Blastophaga psenes (1920a, second edition in 1929a, additional note in 
1935a). In 1936 and 1938, Buscalioni & Grandi wrote two papers on the biology 
and cultivation of Ficus carica, and on the development of its receptacles, in 
relation with the pollinator Blastophaga psenes. The parasite Philotrypesis caricae 
was treated in 1921b (second edition in 1930). In 1961b, Grandi published in 
English on his findings; some of the data mentioned here were taken from that sum- 
mary. Joseph (1958) combined additional notes on B. psenes and new data on 
P. carica, in his thesis. 


The males of Blastophaga psenes emerge from their galls before the females 
do. They approach the galls containing the females, gnaw a hole with the mandibles, 
introduce the tubularly lengthened last segments of the gaster, and fertilize the 
females while they are still in their galls (fig. 4). Each male copulates with several 
females (the sex ratio is 9-18 males for 100 females), and dies within the cavity of 
the fig. The females, after having left their gall through the hole made by the male, 
on their way to the ostiole pass the region of the male flowers where they become 
dusted with pollen. The scales of the ostiole of the D-phase fig (see fig. 1) easily 
yield and allow the females a passage out. The scales lining the ostiole of the 
B-phase figs, where the females now go, offer more resistance: the wasp wedges — 
its head under the free edge of the outer scales, then goes on laboriously through the 
scales and in this process, looses its wings and parts of the antennae and legs. The 
number of females found in the cavity of the young figs seems to vary e.g., Condit 
(1918: 539) mentioned eighteen, Grandi (1929a: 109) found no more than four. 
In the cavity of a gall-fig (see fig. 1), the female may oviposit in as many as 300-400 


Fig wasp research 217 


flowers (in the ovary, between the nucellus and the integument); for some variation. 
see Grandi (1929a: 113). At the same time a small quantity of fluid from the acid 
gland is injected into the endosperm, causing its proliferation into nourishing tissue 
for the wasp larva. The larva passes through two larval stages and a prepupa 
before the pupal stage; complete development takes two-and-a-half, two, or seven 
months, depending on the generation falling in spring, summer, or winter, res- 
pectively (on the number of generations, see Joseph, 1958: 212-216). 


The actions of the females inside the edible or (young) seed-figs are very 
similar to those described above; however, as the long-styled flowers have the 
ovaries out of reach of the wasp ovipositor, the females finally perish after their 
futile attempts to perpuate the species but not before pollination has been accom- 
plished (see a good account in Condit, 1947: 42-46). 


After considering all facts, wrote Buscalioni & Grandi (1936: 117; translated 
from Italian): the symbiosis of Blastophaga and our Ficus is rather complex, and, 
through the intervention of Man, has developed into an association of three 
partners. The Blastophaga and the caprifig can be explained exclusively as a 
parasitic action on the ovules; Man, by practising deceit (“‘mercé un inganno’’), 
succeeded in exploiting the insect, compelling it to enter the receptacles of the 
domestic fig, the flowers of which, long-styled by cultivation, escape infection by 
the insect [end of citation]. It is true that there is a complicated sequence of 
different types of receptacles on the wild fig tree viz., a winter form with mainly 
gall flowers and some male; a summer form with a mixture of gall and female 
flowers, or with female flowers only; and an autumn form with gall flowers 
only, in which the wasps overwinter. Without entering a further discussion here, 
I suggest there is nothing in which the symbiosis of Ficus carica and Blastophaga 
psenes fundamentally differs from symbioses of other dioecious figs and their 
pollinators. As will be shown below, in comparison with many, it even is a rather 
simple instance of mutualistic symbiosis. 


__ Figs. 4-6. Three figures of great historical interest: 4, Blastophaga psenes, male mating 
with female in gall; 5, Philotrypesis caricae, male; 6, Ceratosolen arabicus, female ovipositing 
and pollinating. From Grandi (1920a, 1921b) and Galil & Eisikowitch (1969a). 


218 Gardens’ Bulletin, Singapore — XX1X (1976) 


The generations of Philotrypesis caricae are much the same as in Blastophaga 
psenes. The following account is for a great part taken from Joseph (1966: 
401-402). Copulation of males and females mostly takes place outside the gall, 
soon after the female is liberated by the male from the ovary in which it developed. 
A single male copulates with several females (sex ratio, 50-60 males for 100 females). 
The oviposition will be discussed in the next chapter; about fifty eggs are laid by 
a single female. It seems that the factor determining the oviposition is the presence 
of the acid secreted by the Blastophaga. At the beginning, the larva of both 
Blastophaga and Philotrypesis feed on the endosperm, but later the Blastophaga 
is starved by the Philotrypesis — or may be weakened by some toxic secretion 
produced by the Philotrypesis. This explains much of the unisexual variation in 
size of the imagines, as the quantity of food left for the Philotrypesis-larva depends 
on whether the Blastophaga is being killed early or late in the second instar. This 
may also influence the sex ratio: it has been suggested that haploid males are 
able better to survive partial larval starvation than do diploid females. 


Wasps in Symbiosis (the period after Joseph, 1958) 


In my opinion, Joseph’s doctor’s thesis (Joseph, 1958), discussed in the previous 
chapter, opened a new period in the history of fig wasp research. Joseph knew the 
edible fig and its symbionts as well as Grandi did, but he moreover gained an 
intimate knowledge of the biology of the tropical forms and their parasites. Many 
proved new to science, and thus it took Joseph, as it later did also me as well as 
Hill and Ramirez, much time to describe the new genera and species: a task still 
unaccomplished. Gradually, however, a new classification of fig wasps arises, 
enabling a comparison of the classification of Ficus and the underlying hypotheses 
(Corner, 1965, 1967-1975) with the phylogenetic classification of the wasps. 


THE POLLINATORS 


Soon, the specificity of the relationships between figs and wasps (here taken 
in the restricted sense: Agaonidae only) appeared to be very strict. This was 
already surmised by Grandi earlier, but it could not be proved before a botanist 
and an entomologist, in a joint effort, studied a great many species. Corner started 
this cooperation with Van der Vecht (1959; collections made in Java), from whom 
I took over the entomological part. I started with a revision of the Indo-Australian 
species of Ceratosolen Mayr and Pleistodontes Saunders (Wiebes, 1963a, b). Hill, 
who collected in Hong Kong, and later also in Uganda, began on a revision of 
Hong Kong figs and wasps (Hill, 1967a, b, d), and monographed Liporrhopalum 
Waterston (Hill, 1969). Ramirez collected fig wasps in the Americas; he revised 
Pegoscapus Cameron (Ramirez, 1970a). Later, I would add revisions of the 
genera Alfonsiella Waterston (Wiebes, 1972b), Elisabethiella Grandi and Nigeriella 
Wiebes (Wiebes, 1974a), Agaon Dalman and Allotriozoon Grandi (Wiebes, 1974c), 
while those of Deilagaon Wiebes and Waterstoniella Grandi are in preparation. 
This, it should be noted, still leaves large groups to be revised e.g., African 
Ceratosolen, Eupristina Saunders, the many species united in Blastophaga s.l., 
American Tetrapus Mayr. Large collections exist: see table 6. 


In 1973, I divided the Agaonidae into two subfamilies viz, Agaoninae and — 
Blastophaginae; later again in 1974a, I compared the classification of the genera — 
with that of their host groups of Ficus. This led to a suggestion of a possible — 
classification of the figs into a number of groups different from those used by © 
Corner (1965) but coinciding with the (supposedly phylogenetic) groups of the 
wasps (see table 8). One example will be discussed at the end of this chapter. 


Fig wasp research 219 


Table 6. Important collections of fig wasps made since 1950. 


provenance collector Fieus by some references 


Asia, Australasia Corner Corner Corner, 1958, 1963¢ 
a Bishop Museum - Wiebes, 1976 
India Joseph Joseph Joseph, 1952 ff. 


Wiebes, 1961b ff. 
Corner, 1964 
Wiebes, 1965a, 197ha 
Petersen, 1966 
Hill, 1967a, a 
Corner, 1967 
Petersen, 1966 


Van der Vecht 
Corner 

Wiebes & Pancho 
Noona Dan 
Hill 
Corner 
Noone Dan 


Corner 
Corner 
Corner 


Indonesia, mainly Java 
N. Borneo (Kinabalu) 
Philippine Is. 

a 
Hong Kong 
Solomon Is. 


Hill 
Corner 


Malegasy Blommers Blommers Wiebes, 1974¢ 

La Réunion Etienne Cadet - 

East Africa Galil Wiebes, 1964b, 1968a 
Uganda Hill Wiebes, 1972b, 197hc 
Guinea (W. Africa) Lamotte & Roy Joseph, 1959a 
Nigeria Medler Mrs. Medler Wiebes, 1972a ff. 


Ramirez, 1970a 
Gordh, 1975 


Ramirez 
Remirez, Gordh 


Central America 


Ramirez 
Ramirez, Gordh 


_ Ramirez (1974) took another course, basing himself on the same old table 
(Wiebes, 1963a: 101, table 2) and host catalogue (Wiebes, 1966b) as revised 
later by Hill (1967c: 427, table), but he added an interesting discussion of many 
concurrent characters of Agaonid genera and Ficus-subgenera and sections. This 
new approach became possible, as new data were known on the biology of figs and 
wasps. 


As usual in biology for too long a time, the one instance of Blastophaga 
psenes and Ficus carica taken from the temperate region, was considered to 
present a good example of the symbiosis of figs and wasps in general. The situation 
in the edible fig, however, appeared to be quite simple compared to the pollination 
process in several tropical species. In Blastophaga psenes, the pollen is passively 
carried on the body of the female wasp (“‘topocentric pollination” sensu Galil, 
1973a). As Galil and his coworkers, in many papers of very high standard from 
1965 onwards, have shown, the situation is not always as simple in other Ficus 
species, where “‘ethodynamic pollination” may occur. There proved to be a 
considerable variation in structure and behaviour of the pollinators of different 
species of Ficus. Unique organs used as containers by various species of wasp, for 
transporting pollen from male figs to young receptive female figs (c.f. fig. 6), were 
independently but almost simultaneously, recorded by Ramirez (7.ii.1969, ‘‘corbi- 
culae’’), Galil & Eisikowitch (9.v.1969, “‘pollen pockets’), and Chopra & Kaur 
(3.vi.1969, “‘pollen stuck to the epimeral region of the mesothorax’’). In common 
consent of Galil, Ramirez, and Eisikowitch (1973: 176, note), the name “‘corbiculae”’ 
is used for the pollen-carrying organs on the fore coxae (‘‘coxal corbiculae”’ 
sensu Ramirez), while for the more complicated thoracal organs the term 
“pockets” is used (‘‘sternal corbiculae’”’ sensu Ramirez). In spite of numerous 
Structural differences between the syconia of dioecious and monoecious figs, the 
two may have several biological features in common (Galil, 1973b: 309). In 
table 7 I list the species of fig and pollinator on which we have information 
concerning the pollination process (except for some discussed above), with the 
literature-references added. As in previous sections, in the following compilation 
of what is known on fig-wasp behaviour in various figs, some important parts 
are verbally taken from the original reports. 


220 Gardens’ Bulletin, Singapore — XX1X (1976) 


_ Table 7. Pollination and/or oviposition behaviour described for monoecious (m) and 
dioecious figs (d). 


mostra 


Ficus macrophylla (m) | Pletstodontes froggattt Froggatt, 1901; Pemberton, 1921 


Ficus religiosa (m) Blastophaga quadraticeps | Galil & Eisikowitch, 1965, 1968¢, 1971; 
Galil & Snitzer-Pasternak, 19703 
Galil, Zeroni & Bar Shalom, 1973; 

see also Johri & Konar, 1956 : 


Galil, Ramirez & Eisikowitch, 1973 
Galil, Ramirez & Eisikowitch, 1973 


Ficus costaricana (m) | Pegoscapus estherae | 
Ficus hemsteyana (m) 
PHARMACOSYCEA 

Fieus spp. (m) 
FICUS 

Ficus cartca (a) 

Fieus hirta (da) 

Ficus auriculata (a) 

Ficus nota (a) 

Ficus hispida (4) 

Ficus fistulosa 
SYCOMORUS 

Ficus racemosa (m) 


Pegoseapus tonduzt 


Tetrapus spp. Ramirez, 19702 


Grandi, 1920a, 1929a; Joseph, 1958 
Treub, 1902 
Cunningham, 1889 
Baker, 1913; Williams, 1928 
Lee & Tan, 1973 

Galil, 1973b 


Blastophaga psenes 
Blastophaga javana 
Ceratosolen emarginatus 


2) 


Ceratosolen notus 
Ceratosolen s. solmst 
Ceratosoten hewitte 


Chopra & Kaur, 1969 3) 
Galil, 1966; Galil & Eisikowitch, 
1968a, b, 1969a, 1971, 197 


Ceratosolen fusetceps 


Ficus sycomorus (m) Ceratosolen arabicus 


1 See Ramirez (1970a) for further details on Pegoscapus-behaviour. 
2I am not sure that Cunningham’s observations refer to this species of wasp. 


3 Ficus tsiela with Maniella delhiensis, Ficus virens with Blastophaga vaidi [sic!], and Ficus 
carica with Blastophaga psenes were also mentioned but no details were given. 


Galil & Eisikowitch (1968a: 262-265, fig. 6) distinguished between the 
developmental phases of Ficus sycomorus as follows (see fig. 2): 


Phase A (pre-female). — young syconium prior to the opening of the ostiole. 


Phase B (female). — ostiolar scales loosen, female flowers ripen, sycophilous 
wasps penetrate into the syconium and oviposit into the ovaries; pollination of the 
female flowers. 


Phase C (inter-floral). — wasp larvae and fig embryo’s develop within their 
respective Ovaries; Ovaries occupied by the larvae are transformed into galls. : 


Phase D (male). — male flowers mature, wasps reach the imago stage, fertilized 
female wasps leave the syconia via channels bored by the males. 


Phase E (post-floral). — both the syconia and the seeds inside them ripen. 


Ceratosolen arabicus and the monoecious Ficus sycomorus (see Galil & 
Eisikowitch, 1968a, b, 1969a, b, 1974). — In two phases viz., the female phase B 
and the male phase D, the sycophilous wasps are active within the syconium. In 
the last-mentioned male phase, the male flowers at first remain closed, while the 
male wasps emerge from their galls, puncture the walls of the female galls and 
impregnate the females within. Then, the males assemble at the upper part of the 
syconium: at the end of the first day, the amount of liquid in the syconium ~ 
decreases and the stamens gradually protrude from their perianths at the male 
zone of the fig around the ostiole. 


In the morning of the second day, the male wasps start working at the male 
flower zone: they clasp the anthers and tumble down into the cavity of the fig — 
while still holding the anthers between the legs. At the same time, the female 
wasps start to emerge from their galls, they approach the cut anthers and grasp 
them. With the mandibles and with the scapes of the antennae, a female widens 
the narrow dehiscence slit of the anther, and with the arolia of the fore leg lifts 


Fig wasp research 221 


pollen on to the ventral surface of the body. Then, the wasp curves the thorax 
so that the covering membranes of the pollen pockets stand out along their 
inner suture: a wide opening now leads into the pocket. The pollen is shoveled 
into the pocket with the combs of the fore coxae. 


In the mean time, the males have made tunnels, one to three per syconium, 
in the male flower zone close to the ostiole. Through these tunnels, the females 
eventually emerge, their pockets loaded with pollen. 


The pollination act in Ficus sycomorus is here described after Galil & 
Eisikowitch (1969a), while some details were taken from their 1974 paper. Imme- 
diately upon entering the young syconia at the female phase (B), the female of 
Ceratosolen arabicus starts ovipositing into the pistils, one after the other. Toward 
the end of the oviposition, the fore Jegs of the wasp fold back until the arolia 
reach the lower margin of the pockets (fig. 6). Then, the tarsi touch the stigmata 
below, and so bring the pollen grains on them. 


Ceratosolen hewitti and the dioecious Ficus fistulosa (see Galil, 1973b). —— 
Here the wasp-releasing D-phase male figs and receptive B-phase figs of both sexes 
grow on different trees. The behaviour in the D-phase does not differ essentially 
from that of C. arabicus in F. sycomorus. Also the behaviour of the females on the 
short- and long-styled female flowers (in different figs) is almost identical, although 
eggs are not likely to be laid through the long-styled pistils of the female flowers. 


Blastophaga quadraticeps and the monoecious Ficus religiosa (see Galil & 
Eisikowitch, 1965, 1968c; Galil & Snitzer-Pasternak, 1970, 1971; Galil, Zeroni & 
Bar Shalom, 1973). The behaviour of the wasps is somewhat different from 
that in Ceratosolen arabicus in that the males, after the copulation act, do not cut 
the anthers as the Ceratosolen-wasps do. The fertilized females remain in their 
galls for many hours. In the mean time, the males bore the exit holes, and only after- 
wards do the females begin to emerge. In a series of beautiful experiments, Galil and 
coworkers proved that it is the replenishment of the internal atmosphere by air 
from outside the syconium — lowering the CO.-content to less than 3-4 percent — 
that enables the females to leave their galls. At the same time, this lower CO.-content 
inactivies the male wasps. The diagram of fig. 7 illustrates the reciprocal relationships 
(after Galil, Zeroni & Bar Shalom, 1973: 1122, fig. 7). 


SYCONIUM WASP-POLLINATOR 


Climoctetic 
t 
02- 
incipient -soft 
Modified int. 
atmosphere arse 
Gnrae Q inoctive 
patie "edn lt By heen 
Copulation 
D4 a 04 
Softening Air fe! 3 tunnel 
Cec, 
Yes, a 
£0, 
0600 leave galls 
Ripening 07 lood pollen 
Growth 08 leave tig 
Senescence 


Fig. 7. Reciprocal relationships between the fig and the pollinator in Ficus religiosa. 
From Galil, Zeroni & Bar Shalom (1973). 


222 Gardens’ Bulletin, Singapore — X XIX (1976) 


Now, the females approach the still intact anthers and — here as in Ceratosolen 
arabicus, with the antennal scapes and the mandibles — crumble the pollen. The 
fore tarsi touch the anthers, and the pollen pockets are loaded. Also the unloading 
of the pollen and the act of pollination, in the B-phase young figs, are the same for 
Blastophaga quadraticeps and Ceratosolen arabicus. 


Pegoscapus tonduzi (and P. estherae) and the monoecious Ficus hemsleyana 
(and F. costaricana) (see Galil, Ramirez & Eisikowitch, 1973) —— The wasps of 
most species of the genus Pegoscapus do not have thoracal pollen pockets only, 
but coxal corbiculae as well. As in Ficus religiosa, the female wasp after leaving its 
gall, approaches the male flower and pushes its head between the pistils in search 
for open anthers. The flagella of the antennae are pressed into the anther, while 
the scapes keep open the dehiscence slit. In these species again, the pollen is 
taken with the fore arolia and brought on the mesosternum, where the pollen 
pockets not being completely covered as in the previously mentioned species, 
receive the pollen as it is shoveled in with the coxal comb. Also the coxal corbiculae 
act as pollen containers during the transport to a young fig, after the females have 
left the D-phase syconium through exit holes gnawed by the males. 


The pollination act by P. estherae was divided by Galil, Ramirez & Eisikowitch, 
into the following steps. 1, preparatory step: oviposition; 2, combing of pollen from 
pockets to corbiculae: pollination now starts; 3, transfer of pollen from coxal cor- 
biculae to the arolia of the fore legs; and 4, pollination proper: the striking of 
the fore tarsi on each other, and shaking off the pollen on the stigmata below. 


I discussed the data on pollination in Ficus at some length, because they are 
of the greatest interest for the understanding of the symbiosis of figs and wasps. 
Hopefully, this compilation will stimulate further research and completion of our, 
as yet very incomplete, knowledge of the situation in many groups: “so as to obtain 
a broader view of the evolution of the interrelations between the figs and their 
pollinating wasps” (Galil, Ramirez & Eisikowitch, 1973: 183). 


At this time, the taxonomic implications are not yet very clear. On the one 
hand, the shape and structure of some of the organs used in emerging from the 
galls, pollination within figs, or in entering the young syconia, were used for the 
distinction of the two subfamilies of the Agaonidae (Wiebes, 1973) viz., the elongate 
head and the subvertical orientation of the female mandible (Agaoninae); the 
ventral crenulations (Agaoninae) or ridges (Blastophaginae) on the mandibular 
appendage, which is rigidly (Blastophaginae) or rather loosely connected (Agaoninae) 
to the mandible proper; the prominent and articulate elongation of the third 
antennal segment, more distinctly developed with the Blastophaginae than with the 
Agaoninae; etc. (but see Ramirez, 1974, who finds other connections). On the 
other hand, in one genus (e.g., Pegoscapus, Pleistodontes, Waterstoniella) pollen 
pockets and/or corbiculae may be present in some but absent in other species, 
indicating that a resemblance in pollination behaviour may be the result of conver- 
gent evolution. Tetrapus seems to be primitive in several aspects (Ramirez, in litt.) 
e.g., it lacks external pollen-carrying structures (the pollen is eaten, and carried in 
the digestive tract; Ramirez, 1970b), and it also is the only Agaonid not breaking 
wings and antennae while entering the young syconium. Also in Pleistodontes, the 
condition without pockets may well be primitive, while their presence (e.g., in 
P. froggatti, imperialis) may be a derived character. In some of the Blastophaginae, 
however, the external pollen-carrying structures seem to be secondarily lost (e.g., 
in some Waterstoniella), or are in the process of being lost (as in Waterstoniella — 
masii). | 

What is needed for a reconstruction of the coevolution of figs and wasps, is a 
more complete survey of character-states in many groups, permitting of a phylo- — 
genetic analysis. The groups to be prospected include all symbionts of the fig, 
inquilines and parasites (in short: mess-mates) as well as pollinators. The symbioses, 
then, are taken as the taxonomic units of the phylogenetic classification, while the 


' 


Fig wasp research 223 


wasps (with all their features) are treated as the characters of the symbiosis. 
Although some classification on the tribal level was recently suggested, and accepted 
by students of fig insects (see table 4), the knowledge of the mess-mates is as yet 
very scanty’). A survey of some, mostly biological data is presented below. 


THE MESS-MATES 
A gaonidae 


The symbioses of figs and wasps have other partners than pollinators and 
plants. Recently, it became known that some of the Agaonidae behave as 
cuckoos: laying eggs without preparing food (i.e., pollinating the flowers!). The 
first and best known instance is Ceratosolen galili in Ficus sycomorus (see Wiebes, 
1964b, 1968a; Galil & Eisikowitch, 1968a, 1969a). The female has pollen pockets 
and its behaviour during oviposition is quite similar to that of Ceratosolen arabicus: 
the pockets are always empty, however, and pollination movements have not been 
observed. In a way, its behaviour is similar to that of Sycophaga sycomori (at 
least, its place in the symbiosis is). In my opinion, C. galili is not closely related 
to C. arabicus. This poses the question as to the evolution of its relationship with 
the sycomore fig. As seen from its pollen pockets, C. galili in a previous evolutionary 
stage acted as a pollinator, but to which fig? If it is conceivable that two species 
of fig merge, keeping one of the pollinators as such while the other is lost or 
develops into a food-parasite; or that a species of wasp switches from its ‘“‘own”’ 
fig to another, to act as a parasite — what about the supposed phylogenetic speci- 
ficity of figs and wasps? 

Several instances of supposed parasitic Agaonidae are now known, mainly 
from Africa. A previously recorded case of an Indo-Malayan fig harbouring two 
Agaonidae (Wiebes, 1966c) should be reconsidered in the light of our new 
knowledge. Also the instance of two species of Pegoscapus-symbionts of Ficus 
tuerckheimii in Costa Rica (Ramirez, 1970a) should be reinvestigated. Some more 
species of Ceratosolen seem to belong to the group of C. galili e.g., flabellatus, which 
lives in the syconia of Ficus capensis next to what I suppose to be the legitimate 
partner (C. capensis). Some species of Alfonsiella are sometimes found in figs 
evidently pollinated by other wasps (i.e., Elisabethiella; Wiebes, 1972b): a male 
of Alfonsiella was found next to one of Elisabethiella in Ficus salicifolia by 
Mayr (1885: 192), and it was mistaken for an apterous form of Crossogaster 
triformis (see Grandi, 1928d: 206-210; Wiebes, 1975). More often than not, 
however, the species of Alfonsiella are found quite alone, and they do have 
pollen pockets. 


Toryminae 

Physothorax, from figs of section Americana, was recently recognized as one 
of the Toryminae (Burks, 1969). The females have long ovipositors, with which 
they pierce the fig receptacle from the outside (Butcher, 1964: 237). There are 
winged as well as wingless (or brachypterous) males. 


Sycophagini 

Sycophaga sycomori is one of the Sycophagini, a tribe of the Torymidae 
Sycophaginae (see table 4). Sycophaga contains a number of species all of which, 
as far as known or assumed from their morphology, enter the figs of African 
Sycomorus through the ostiole to oviposit. S. sycomori is able to induce the 
formation of parthenogenetic nourishing tissue for its larva. This tissue, however, 
Originates in the nucellus and not in the endosperm as in Ficus carica (see 
references in Grandi, 1929a: 112) or in Ficus religiosa (Johri & Konar, 1956). 


1 Hill (1967d: 95) listed ten genera as “incertae sedis”. Some of these were mentioned above 
(viz., nos, 1, 2, 6, 7, 8, 9): which leaves only four unplaced viz., Critogaster Mayr (American 
parasites of Tetrapus), Dynatogmus Mayr from Africa, Heterandrium Mayr (American 
parasites of Pegoscapus) and Pseudidarnes Girault from Australian Malvanthera. 


224 Gardens’ Bulletin, Singapore — X XIX (1976) 


The behaviour of Sycophaga sycomori, and its effects on the structure and develop- 
ment of Ficus sycomorus, were discussed by Galil, Dulberger & Rosen (1970; 
see also the papers by Galil & Eisikowitch mentioned with F. sycomorus, above). 


The females of most Sycophagini have long ovipositors, and they oviposit from 
the outside of the fig, through the peel. Ansari (1966: 80-82, Parakoebelea; 1967: 
380-381, “Idarnes’’) described the process of egg-laying in Sycophagine wasps 
(see fig. 8a, b). After locating a proper place on the surface of the fig, the female 
moves forward in order to bring the distal end of the ovipositor near the selected 
place. Holding the fig firmly with its legs, the female moves its ovipositor forward 
and backward till the surface of the fig is punctured; then, the insect creeps 
backward, pushing the ovipositor (guided by the valves, from which it gradually 
dislodges proximally) into the fig receptacle. Usually, one egg is deposited into 
each gall flower, but in some cases two eggs were laid: it is worth mentioning 
that Ansari recorded the finding of two specimens viz., a male and a female 
developing within a single gall — in my opinion, this record wants confirmation. 
The males of the Sycophagini are rather aberrant. Grandi (19l6a: 227-228, 
figs. 32, 1; 36, 2; etc.) described the peculiar transverse division of the head into 
two parts, the anterior of which bears the eyes, the antennae, and the sockets for 
the mandibular condyles. The gaster bears very long, laminate excrescences of the 
spiracles of the eighth urotergite. The morphology of the male Jdarnes (Ganosoma 
in Mayr’s sense) recently redescribed by Gordh (1975: 408-412), shows that its 
relationship to the Old World Sycophagini cannot be very close as e.g., the head 
is relatively normal, and the spiracles of the eighth urotergite have no excrescences. 


a Cc 


Fig. 8. Some stages in the process of oviposition in Sycophagini (a, b), Sycoryctini (c, d), : 
ase ben (e, f), and Apocryptini (g, h). Adapted from Joseph (1953a, 1958) and Ansari 


Ansari used the term ‘‘cleptoparasite’’ for the wasps discussed, and Hill — 
(1967c: 431) suggested that the species of Eukoebelea are phytophagous and — 
compete with the Agaonidae for the ovule endosperm. In young receptacles of 


Fig wasp research 225 


Ficus nota in the Philippines, I saw Eukoebelea ovipositing (? no eggs observed!) 
before Ceratosolen had entered the fig. 


Eukoebelea has been recorded from sections Neomorphe and Sycocarpus, and 
from subgenus Sycomorus (see the plant groups mentioned in table 8); the 
genus /darnes is restricted to section Americana (see Gordh, 1975), while the Old 
World species alluded to this group have a rather wide host-spectrum; Parakoebelea 
is known from Indian and African Sycomorus (and one species from section 
Conosycea?); while Sycophaga only occurs in African Sycomorus. In general, 
most Sycophagini (“Jdarnes’’ excluded) appear to be living in figs pollinated by 
Agaonidae of the genus Ceratosolen, and by those of Pegoscapus. 


Apocryptini 

Again, reference should be made to the paper by Ansari (1967). Apocrypta 
westwoodi, like all congeners, is peculiar in having the female gastral segments 
keeled, permitting of a telescoping lengthening of the gaster. The insect, in 
drilling a hole through the peel of the fig, raises its hind pair of legs, and the 
Ovipositor is pushed in, beneath the body of the wasp (fig. 8g). The ovipositor 
gets lodged in the grooves formed by the gastral sternites. Now the legs are 
relaxed; the valves still guide the ovipositor until, after thrusting a considerable 
length of the ovipositor, the wasp suddenly pulls out the valves, which now rest 
over the fig or swish in the air (fig. 8h). The male (Grandi, 1916a: 264-273) is 
slender, and has large — although never protruding — spiracular peritremata of 
the eighth urotergite. 


The species seem to be restricted to Ceratosolen-harbouring figs viz., Neo- 
morphe, Sycocarpus and Sycomorus. Presumably, A. longitarsus parasitizes (or 
lives as an inquiline with) Sycophaga sycomori in Israeli Ficus sycomorus (Galil & 
Eisikowitch, 1968b: 757). It is peculiar, and well worth further research, that 
some related forms from African figs are much larger and more robust, in the 
same relation to normal Apocrypta as Parakoebelea stands to Eukoebelea. 


Sycoryctini 


The Sycoryctini form a large tribe, the internal relationships of which are not 
very clear. In the Sycoryctini, the apparent gaster ends with the eighth urotergite, 
and the ninth is tubularly lengthened covering the valvulae almost to the tips 
(forming a “‘tail’’). Joseph (1953c: 67-69) described the process of oviposition 
for Sycoscapteridea (fig. 8c, d). When the female feels a particular spot to be 
Suitable, the tip of the “‘tail’’ is brought in contact with the surface, which is 
pierced. As the insect creeps backward, the ovipositor, dislodged from the 
sheathing “‘tail’’, is thrust into the fig. After oviposition, the wasp pulls out the 
Ovipositor in an interesting manner: it slowly raises the gaster by straightening 
its bent legs and gently pulls out the ovipositor stage by stage, while slowly 
creeping forward till the whole ovipositor is out of the fig. The males are less 
depressed or slender than in the Sycophagini or Apocryptini, respectively; the 
head is not divided into two parts, and the spiracular peritremata are not 
prominent, nor very large. 


The Indo-Australian genera were keyed by Wiebes (1967e: 173). They are 
generally found throughout the subgenera Urostigma and Pharmacosycea (both, 
Old World species only), and Ficus, but not occurring in all species. Hill (1967c: 
431) noted that they may well be parasites of the Agaonidae or even of the other 
Sycophaginae, as they are noticeable smaller than the other wasps in their respective 
fig faunas. 


Philotrypesini 
The cleptoparasite of Blastophaga psenes in Ficus carica is a member of this 


tribe; its oviposition-behaviour was studied by Joseph (1958) while earlier observa- 
tions, with a figure of ovipositing female wasps, were given by Lichtenstein (1919, 


226 Gardens’ Bulletin, Singapore — XX1X (1976) 


figs. 2-3). With the females of the Philotrypesini, the eighth and ninth gastral 
segments are modified, and they form part of a “‘tail”; moreover, the ovipositor 
proper and its valves are rather long. Here again, as in the Apocryptini, the gaster 
is raised high, and the wall of the fig is pierced almost beneath the body of the 
wasp (fig. 8e, f). Then, the ovipositor is dislodged from its sheath. According to 
Joseph (1958: 225), the valves remain at the point of insertion of the ovipositor, 
and they are not kept backward as Lichtenstein (1919: 316) recorded; only in 
case of disturbance, the valves are kept ‘‘en position de repos’. The males of 
Philotrypesis (fig. 5) show some superficial resemblance to those of the Sycoryctini, 
but they may — among other things — be easily distinguished by the emarginate 
ventral stomal edge. Some species have fully winged (““Shomomorphic’’) males, and 
several intermediate forms may occur in one sample (for these and other variations, 
see Grandi, 1930: 53-71). 

The species occur in Old World groups of Urostigma, Oreosycea and Ficus. 
Sycomorus has no Philotrypesis. 


Otitesellini 


The females have a short ovipositor, and for that reason are supposed to 
oviposit from within the fig receptacle. Some have special features evidently related 
to the way of entering the fig e.g., rasp-like regions on the thorax (Eujacobsonia), 
stout teeth or spines on the legs (Grasseiana, Lipothymus), etc. The males are 
peculiar by their oversized heads and mandibles, and they superficially resemble 
those of Philotrypesis. The hosts are found in the Old World groups of Urostigma 
(Malvanthera excluded), Oreosycea, in a few species of Sycidium, and one of 
Sycocar pus. For a review, see Wiebes (1974d: 161). 


Sycoecini 

Several of these were formerly classified with the Sycophaginae in the old 
sense, until Hill (1967d: 94-95, 98) erected a separate tribe for their reception. The 
females have several adaptations for penetrating the fig ostiole, especially in various 
appendages to the mandibles or the fore tibiae (see also the remarks on Seres, by . 
Ramirez, 1974: 774, 776). The males are alate. The distribution of the group is 
disjunct, one genus (Diaziella, see Wiebes, 1974b) occurring in the Philippines 
(presumably in some figs of section Conosycea), while all others are African (host 
figs of section Galoglychia, and one in section Urostigma). 


Epichrysomallinae 


Several genera, some of which with a complicated taxonomic history having 
been classified with several Chalcidoid families, were recently united in this sub- 
family (see Hill, 1967d: 96-98). Since then, three new genera were added viz., 
Parasycobia and Sycobiomorphella by Abdurahiman & Joseph (1967b), and 
Sycophilomorpha by Joseph & Abdurahiman (1969). The species occur mostly in 
Urostigma-figs, but one was recorded from Ficus ampelas, another from F. tincto- 
ria (both, section Sycidium): it is on these that some biological data are available. 
Females and males of Neosycophila omeomorpha Grandi (see 1923d), both fully 
winged, develop in large galls of Ficus tinctoria gibbosa, which they eventually 
leave to the outside of the receptacle. Grandi (p. 114) stated as a peculiarity (for 
fig wasps!) that the male has not developed any “‘incarico per la liberazione della 
sua compagna”’ with which, of course, it mates outside the fig. 


Eudecatominae 


Of the fig wasps not belonging to either the Agaonidae or the Torymidae, this — 
is the most important group. Many species were described from figs of the subgenus — 
Urostigma, from Asia as well as from South America: these include several, 
originally classified with Decatoma (some differential characters of Eudecatoma 
and Sycophila, as most are now named, were given by Burks, 1971: 7). Boucek 
(1974: 268) noted that there seems to be little information about whether the - 


. 


Fig wasp research 227 


sycophilous species are really confined to figs, as several others do develop in 
various galls on other plants, or are clearly associated with insects in grass stems. 
Joseph (1959b: 92) suggested a “‘cleptoparasitic’’ way of life for Decatoma fici in 
Ficus virens; Hill (1967c: 431) noted that Sycophila are probably phytophagous 
gall-formers, although they could be parasitizing the Epichrysomallinae. The struc- 
ture of the female reproductive system was discussed by Copland & King (1972). 


THE FIGS 


In the lowland tropics of Asia and Australasia, the abundance of fig-species 
is a good measure of the richness of the environment in plant and animal life 
(Corner, 1967: 24, see also p. 32 ff.). Ficus is mainly defined by its syconium (i.e., 
in my opinion, by blastophagy), and this conceals the fact that Ficus has greater 
diversity in vegetative mechanism than any other genus of flowering plant and, 
indeed, of most families. From this basis, one expects a rather clear picture of the 
taxonomic subdivision of the genus, once the species are described and the 
synonymies revealed. Much as Ficus can be taken as an example of the phyloge- 
netic history of its biota, the classification of its hymenopterous symbionts should 
conform. Indeed, most of the series and sections as defined by Corner (1965), prove 
to be paralleled by groups of wasps, especially those of the pollinating Agaonidae. 
The larger subdivision of Ficus in four taxonomic sections, however, is not in all 
parts reflected in the composition of the wasp fauna (table 8). 


Table 8. The classifications of figs and wasps compared. 


Allotriozoon, Elisa- 
bethtella, Nigertetla 
Pegoscapus 


Ficus Agaonidae 
| Agaoninae Blastophaginae | 
| UROSTIGHA See Poe Og ee 
Urostigna | Eltsabethielta ') | -Blastophaga | 
Leueogyne | | Maniella | 
Conosycea | Blastophaga, Euvristina, 
Parapristina, Waterstoniella, | 
Detlagaon | 
Stilpnophytlum | Blastophaga 
Malvanthera Pleistodontes Blastophaga ') 
: ° . | 
| Galoglychia 4gaon, Alfonstella, | 
| 
| 


’ 
| 
| 


Blastophaga, Dolichoris 


Ficus | 
) Ficus Blastophaga | 
| Phizocladua | Blastophaga 
Xalosyce ' Blastophaga | 
| Sinosycidiun | ? | 
Syctdiun Iiporrhopalum, Ceratosolen 
| Adenosperma Ceratosolen 
Neomorphe ) Ceratosotlen 
) Sycocarpus ) Ceratosoten 


1 One species only; these records need confirmation. Several other, solitary, records of figs 
and wasps of uncertain classification are omitted. 


228 Gardens’ Bulletin, Singapore — XX1X (1976) 


A notable discrepancy, here discussed as one example of the joint effort of 
botany and entomology to arrive at an integrated classification, is found in the 
group pollinated by Ceratosolen-wasps viz., sections Adenosperma, Neomorphe 
and Sycocarpus of subgenus Ficus, and subgenus Sycomorus. Also with the mess- 
mates, three of these groups are exclusively characterized by the presence of one 
genus viz., Apocrypta, while one, Sycomorus, is characterized by the presence of 
Sycophaga (in Africa) and the absence of Philotrypesis. Some of the species classi- 
fied with Ceratosolen (but none of Apocrypta and Sycophaga), are members of the 
entomofauna of other fig sections e.g., section Sycidium (Ficus minahassae with 
Ceratosolen pygmaeus; F. pungens with C. nanus); section Ficus (F. pseudopalma 
with C. bakeri); section Oreosycea (F. pritchardii with C. marshalli). Ramirez 
(1974), referring to his unpublished thesis, combined these species and groups, as 
well as F. rivularis (‘probably pollinated by a Ceratosolen wasp’’), all in a heap 
(subgenus Sycomorus in his sense). When I classified Ceratosolen marshalli, nanus, 
and pygmaeus (Wiebes, 1963a: 8-9, 85; two other species, from figs of section 
Sycocarpus, were tentatively placed in the same species-group), I did not know 
Liporrhopalum. Now, having at hand Hill’s revision of Liporrhopalum, many of 
its characteristic features lead me to a revaluation of the three putative Cerato- 
solen’s. Not all connections are clear yet, mainly because most groups of Blasto- 
phaga s.l. are still not revised, but I cannot now be as certain as I was twelve years 
ago, of any apparent affinity with Ceratosolen. As to the botanical place of Ficus 
pritchardii, a “‘problem is that, as a monoecious species [it] should belong in one 
of the subgenera Urostigma, Pharmacosycea or Sycomorus. It fits none and finds 
no aberrant alliance with any of their species” (Corner, 1970b: 401). 


Ficus pseudopalma (as well as F. rivularis) differs from the rest of section 
Ficus markedly enough to require a separate taxonomic series (Corner, 1969b: 
326); on p. 56 of 1967, Corner stated: “‘if F. pseudopalma had an entire perianth, 
which seems a detail, it would be close to F. dammaropsis” (section Sycocarpus). 
In the same paper of 1969 (b, fig. 5) Corner illustrated the intricate relationships 
between sections Ficus and Sycocarpus. In this diagram, Auriculisperma and 
Sycocarpus are derived from an ancestral Ficus, which also sends offshoots to 
section Ficus (with Pseudopalmeae as one of the early branches) and, separately, to 
Rivulares. It does not show Sycomorus, some species of which harbour wasps 
immediately related to those from Neomorphe (e.g., F. oligodon and F. auriculata 
with Ceratosolen emarginatus). F, oligodon, it should be noted, was formerly classi- 
fied with Sycocarpus (subsection Pomifera) because of its saccate perianth covering 
the ovary: a prime respect in the classification of the genus (Corner, 1962: 395). In 
Sycomorus, the one Indo-Australian species (viz., F. racemosa) is peculiar in not 
having a symbiont of the genus Sycophaga, which is present in all African species; 
the figs are monoecious, while the Ficus sections mentioned above are dioecious. 


In my opinion, as also published in 1973 (p. 24-25), the entomological evidence 
suggests a reclassification of the figs although this should wait, I hasten to add, 
until the evidence is more conclusive! The interplay of characters, as recorded in 
Ficus, may possibly be unravelled by the characters of the wasps. As our present 
knowledge of Ceratosolen indicates, the old classification of Neomorphe with 
Sycomorus appears to be confirmed, and its close alliance with Sycocarpus 
(Covellia) corroborated. This is not to suggest that the origin of Sycocarpus is to 
be sought in modern Neomorphe (Corner, 1962: 395, contradicted this), but they 
may form sister-groups which, of course, is what is meant by “alliance” or “‘taxo- 
nomic relationship’. The monoecious condition found in Sycomorus as well as in 
a species of Papuasycea, may indicate the primitive state, whereas Neomorphe and 
Sycocarpus (etc.) may represent the derived dioecious condition. The pollinator of 
Ficus pseudopalma, in my opinion, gives away a close connection with primitive 
Sycocarpus, while the absence of Apocrypta from its entomofauna, may point to 
an early branching. 


Fig wasp research 229 


The completion of a laborious task is still before us: the inventory of the fig 
fauna, and the apprehension of the relations between figs and wasps. The combina- 
tions of characters then, once seen in a phylogenetic context, recognized as 
indicators of monophyletic groups of taxa and, eventually, understood in their 
biological meaning, may be used as arguments for a classification of their bearers: 
figs and wasps in symbiosis. 


References 


For convenience, this list includes only the references not given in Hill’s (1967d: 
107-124) bibliography, a few corrections (indicated by an asterisk), and additions 
to that bibliography. It is supposed to be complete up to and including most of the 
year 1975. 


ABDURAHIMAN, U. C. & K. J. JOSEPH. 1967a. Contributions to our knowledge of fig 
insects (Chalcidoidea: parasitic Hymencptera) from India (New Series) 1. Notes on some 
new and interesting fig-insects— Oriental Insects 1: 1-19. 

1967b. Idem 2. New fig insects from Delhi and correction of a mistaken identifi- 
cation.— Bull. Ent. Loyola Coll. 8: 48-57. 

1975a. Three new Chalcidoidea (Hymenoptera) from India.— Oriental Insects 
9: 99-109. 

1975b. New fig insects (Hymenoptera : Chalcidoidea) from India: three 
Torymids parasitic on Agaonids.— Entomophaga 20: 73-80. 

ANSARI, M. H. 1967. The process of egg laying in Idarninae (Chalcidoidea: Hymenoptera). 
— Ind. J. Ent, 29: 380-384. 

BALTAZAR, C. R. 1966. A catalogue of Philippine Hymenoptera (with a bibliography, 
1758-1963).— Pacific Ins. Monogr. 8: 1-488. 

BOUCEK, Z. en On the Chalcidoidea (Hymenoptera) described by C. Rondani— Redia 
55: 241-285. 

BURKS, B. D. 1969. Redefinitions of two genera of Chalcidoids from figs, with new Florida 
species (Hymenoptera).— Florida Ent. 52: 115-122. 


—————— 1971. A synopsis of the genera of the family Eurytomidae (Hymenoptera: 
Chalcidoidea).— Trans. Am. ent. Soc. 97: 1-89. 

CASTELLANOS, A. 1944. La especie de Ficus del noroeste Argentino.— Lilloa 10: 483-491. 

CHOPRA, R. N. & H. KAUR. 1969. Pollination and fertilization in some Ficus species.— 
Beitr. Biol. Pflanzen 45: 441-446. 

COPLAND, M. J. W. & P. E. KING. 1972. The structure of the female reproductive system 
in the Eurytomidae (Chalcidoidea: Hymenoptera).— J. Zool. (London) 166: 185-212. 


COPLAND, M. J. W., P. E. KING & D. S. HILL. 1973. The structure of the female reproduc- 
ote in the Agaonidae (Chalcidoidea, Hymenoptera).— J. Ent. (London) (A) 48: 

CORNER, E. J. H. 1967. Ficus in the Solomon islands and its bearing on the post-Jurassic 
history of Melanesia.— Phil. Trans. R. Soc. Lond. (B) 253: 23-159. 


——————— 1969a. The complex of Ficus deltoidea; a recent invasion of the Sunda Shelf.— 
Ibid. 256: 281-317. 


1969b. Ficus sect. Adenosperma.—I bid. 256: 319-355. 


1970a. Ficus subgen. Ficus. Two rare and primitive pachycaul species.—I bid. 
259: 353-381. 


1970b. Ficus subgen. Pharmacosycea with reference to the species of New 
Caledonia.— Ibid. 259: 383-433. 


1975. Ficus in the New Hebrides.— Ibid. 272: 343-367. 
CROIZAT, L. 1968. The biogeography of the tropical lands and islands east of Suez- 
Madagascar: with particular reference to the dispersal and form-making of Ficus L., 


and different Ren os vegetal and animal groups.— Atti Ist. bot. Lab. Crittogam. Univ. 
Pavia (6) 4: 1-400. 


“te A proposito di alcune critiche di E. J. H. Corner.— Ibid. 5: 181-190. 


EISEN, G. 1901. The fig: its history, culture and curing, with a descriptive catalogue of the 
known mre of figs—Bull. Div. Pomol. U.S. Dept. Agric. 9: 1-317 [Bibliography: 


230 Gardens’ Bulletin, Singapore — XX1X (1976) 


FORSKAL, P. 1775. Flora aegyptiaco-arabica: 1-32, i-cxxvi, 1-220. 
GALIL, J. 1966. [The sycomore tree in the civilization of the Near East].— Teva VeAreiz 8: 
306-318, 338-355 [Hebrew]. 
1967. Sycomore wasps from ancient Egyptian tombs.— Israel J. Ent. 2: 1-10. 
1968. An ancient technique for ripening sycomore fruit in East Mediterranean 
countries.— Econ. Bot. 22: 178-190. 
1973a. Topocentric and ethodynamic pollination.— Jn N. B. M. Brantjes (Ed.), 
Pollination and dispersal: 85-100. 
1973b. Pollination in dioecious figs. Pollination of Ficus fistulosa by Ceratosolen 
hewitti— Gdns’ Bull., Singapore 26: 303-311. 


GALIL, J., R. DULBERGER & D. ROSEN. 1970. The effects of Sycophaga sycomori L. on 
the structure and development of the syconia in Ficus sycomorus L.— New Phytol. 69: 
103-111. 


*GALIL, J. & D. EISIKOWITCH., 1965. [Pollination of the flowers of Ficus religiosa L.].— 
Teva VeAretz 7: 1-16 [Hebrew]. 


1968a. On the pollination ecology of Ficus sycomorus in East Africa Ecology 
49: 259-269. 

1968b. Flowering cycles and fruit types of Ficus sycomorus in Israel— New 
Phytol. 67: 745-758. 

1968c. On the pollination ecology of Ficus religiosa in Israel Phytomorph- 
ology 18: 356-363. 

1969a. Further studies on the pollination ecology of Ficus sycomorus L. 
(Hymenoptera, Chalcidoidea, Agaonidae).— Tijdschr. Ent. 112: 1-13. 

1969b. Note on pollen transport, pollination and protection of ovaries in Ficus 
sycomorus.— New Phytol. 68: 1243-1244. 

1971. Studies on mutualistic symbiosis between synconia and sycophilous wasps 
in monoecious figs.— Ibid. 70: 773-787. 

1974. Further studies on pollination ecology in Ficus sycomorus ii. Pocket 
filling and emptying by Ceratosolen arabicus Mayr.— Ibid. 73: 515-528. 


GALIL, J., W. RAMIREZ B. & D. EISIKOWITCH. 1973. Pollination of Ficus costaricana 
and F. hemsleyana by Blastophaga estherae and B. tonduzi (Agaonidae) in Costa Rica.— 
Tijdschr. Ent. 116: 175-183. 


GALIL, J. & Y. SNITZER-PASTERNAK. 1970. Pollination in Ficus religiosa L. as connected 
with the structure and mode of action of the pollen pockets of Blastophaga quadraticeps 
Mayr.— New Phytol. 69: 775-784. 


1971. Note on pollination in Ficus religiosa L.— Ent. Ber., Amst. 31: 123-124. 


GALIL, J.. M. ZERONI & D. BAR SHALOM. 1973 Carbon dioxide and ethylene effects in 
the co-ordination between the pollinator Blastophaga quadraticeps and the syconium in 
Ficus religiosa.— New Phytol. 72: 1113-1127. 


GALLESIO, G. 1820. Pomona italiana. Parte scientifica fasc. 1 contenente il trattato del 
fico: 81-103. 


GAUD, S. M. & L. F. MARTORELL. 1973. New insect records for Puerto Rico.— J. Agric. 
Univ. Puerto Rico 57: 247-254. 


GIRAULT, A. A. 1917. Some new Australian chalcid-flies, mostly of the family Encyrtidae 
(Hymenoptera).—Insecutor Inscit. menstr. 5: 29-37. 


GORDH, G. 1975. The comparative external morphology and systematics of the neotropical 
parasitic fig wasp genus Idarnes (Hymenoptera: Torymidae.— Univ. Kansas Sci. Bull. 50: 
389-455. 


GRANDI, G. 1967. La vita straordinaria degli insetti dei fichi— Scientia 7 (102): 7. 
*HASSELQUIST, F. 1757. Iter Palaestinum. Eller Resa til Heliga Landet forrattad ifran At 7 
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1762. Reise nach Palastina in den Jahren von 1749 bis 1752. Auf Befehl © 
Ihro Majestat der Kéniginn von Schweden herausgegeben von Carl Linnaeus: 1-17, 1-606. 
*HEGARDT, C. 1749. Ficus.— Jn Caroli Linnaei Amoenitates Academicae | (2): 23-54. 
HILL, D. S. 1967d, Figs (Ficus spp.) of Hong Kong: i-viii, 1-130 [Bibliography: 107-124]. 
1969. Revision of the genus Liporrhopalum Waterston, 1920 (Hymenoptera 
Chalcidoidea, Agaonidae.— Zool. Verh. 100: 1-36. . 
1971. Wasps and figs— New Scient. & Science J.: 144-146. 


Fig wasp research 231 


HOWARD, L. O. 1899. The present status of the caprifig experiments in California.— Bull. 
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*JOSEPH, K. J. 1957a. Contributions to our knowledge of fig insects (Chalcidoidea: parasitic 
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species.— Ann. Soc. ent. France 125: 97-133. 


1966. Taxonomy, biology and adaptations in fig insects (Chalcidoidea).— Proc. 
2nd All-India Congr. Zool. 2: 400-403. 


1967. Newer trends in the taxonomy of the fig-inhabiting Chalcidoidea.— Bull. 
nat. Inst. Sci., India 34: 257-262. 


JOSEPH, K. J. & U. C. ABDURAHIMAN. 1968. Descriptions of six new species of Decatoma 
(Chalcidoidea : Eurytomidae) from Ficus benghalensis L— Oriental Insects 2: 63-87. 


1969. Contributions to our knowledge of fig insects (Chalcidoidea: Hymenop- 
tera) from India 4. Further descriptions of new fig insects from Ficus bengalensis L.— 
Ibid. 3: 37-45. 


LATREILLE, P. A. 1825. Familles naturelles du régne animal: i-vi, 1-570. 


LEE, S. S. & C. H. TAN. 1973. Fig wasps (Hymenoptera, Chalcidoidea).— Malay. Nat. J. 26: 
112-119. 


LICHTENSTEIN, J. L. 1919. Note préliminaire au sujet de Philotrypesis caricae Hass.— Bull. 
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NIKOLSKAJA, M. N. 1954. [Blastophaga-pollinator of the fig]— Priroda, Leningrad 5: 
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PETERSEN, B. 1966. The Noona Dan Expedition, 1961-62. Insects and other land arthro- 
pods.— Ent. Medd. 34: 283-304. 


PRINCIPI, M. M. 1971. Guido Grandi e la sua opera.— Boll. Ist. Ent. Univ. Bologna 30: 
1-24. 


RAMIREZ B., W. 1969. Fig wasps: mechanism of pollen transfer.— Science 163: 580-581. 


1970a. Taxonomic and biological studies of neotropical fig wasps (Hymenoptera: 
Agaonidae).— Univ. Kansas Sci. Bull. 39: 1-44. 


1970b. Host specificity of fig wasps (Agaonidae).— Evolution 24: 680-691. 


——1— 1974. Coevolution of Ficus and Agaonidae— Ann. Missouri Bot. Gdn 61: 
770-780. 


ROBSON, T. B. 1911. Blastophaga in Australia— Rural Calif. 35: 307. 
SANTIS, L. de. 1971. La fauna de Chalcidoideos de America del Sur.— Bol. Soc. ent. Peru 6: 
59-63. 


*SAUNDERS, S. S. 1883a. Descriptions of three new genera and species of fig insects allied to 
Blastophaga from Calcutta, Australia, and Madagascar; with notes on their parasites 
and on the affinities of the respective races.— Trans. ent. Soc. London: 1-27. 


1883b. [Characterization of fig insects]— Proc. ent. Soc, London: v-vi. 


*—_____ 1883c. On the Cynips caricae of Hasselquist and other fig-insects allied thereto: 
with descriptions of a new species from Australia— Trans. ent. Soc. London: 383-392. 
1883d. [Exhibition of both sexes of Ichneumon ficarius . . . ].— Proc. ent. 


Soc. London: xxxi—xxxii. 
SAVAGE, C. G. 1924. Smyrna fig culture— J. §. Austra. Dept. Agric. 28: 401-421. 
SISSON, R. F. 1970. The wasp that plays cupid to a fig— Nat. Geographic 138: 690-697. 


TREUB, M. 1902. L’organe femelle et l’embryogénése dans le Ficus hirta Wahl.— Ann. Jard. 
bot., Buitenzorg (sér. 2) 3: 124-157. 

VECHT, J. van der, 1973. Insekten zonder tal: een uitdaging.— Versl. Ned. Akad. Wetensch. 
Amst. (Nat.) 82: 41-48. 

WALKER, F. 1846. List of the Hymenopterous insects in the collection of the British 
Museum, part 1: 1-100. 


WATERHOUSE, C. O. 1881. Remarks on the types of Cynips psenes and Cynips sycomori 
in the Linnean Collection— Proc. ent. Soc. London: xli-xlii (and reply by Saunders: 
xlii-xlv). 

WESTWOOD, J. O. 1883c. [Further descriptions of insects infesting figs; errata].— Trans. 
ent. Soc. London: Vii. 

WIEBES, J. T. 1967a. Indo-Malayan and Papuan fig wasps (Hymenoptera, Chalcidoidea) 5. 
Description of Otitesellini (Torymidae).— Proc. Acad. Sci. Amst. (C) 70: 121-136. 


1967b. idem 6. The genus Eujacobsonia Grandi (Torymidae).— Zool. Meded., 
Leiden 42: 107-115. 


232 Gardens’ Bulletin, Singapore — XX1X (1976) 


1967c. Guadalia vissali nov. gen., nov. spec., a new fig wasp from the Solomon 
Islands (Hymenoptera, Torymidae, Otitesellini)— Ent. Ber., Amst. 27: 214-218. 


1967d. Polanisa Walker, 1875 (Insecta, Hymenoptera): proposed suppression 
under the plenary powers.— Bull. zool. Nomencl. 26: 319-320; 31: 24-26 (1974, Opinion 
no. 1018). 


1967e. Redescription of Sycophaginae from Ceylon and India,with designation 
of lectotypes, and a world catalogue of the Otitesellini (Hymenoptera Chalcidoidea, 
Torymidae.— Tijdschr. Ent. 110: 399-442. 


1968a. Fig wasps from Israeli Ficus sycomorus and related East African species 
(Hymenoptera, Chalcidoidea) 2. Agaonidae (concluded) and Sycophagini— Zool. Meded., 
Leiden 42: 307-320. 

1968b. Species of Agaon from Congo (Kinshasa), with notes on synonymy 
(Hymenoptera, Chalcidoidea).— Proc. Acad. Sci. Amst. (C) 71: 346-355. 

1968c. A new Pleistodontes (Hymenoptera Chalcidoidea, Agaonidae) from 
Rennell Island Nat. Hist. Rennell Isl. 5: 115-117. 


1969a. Preliminary report on a collection of fig insects (Hymenoptera 
Chalcidoidea) from Ficus gnaphalocarpa.— Mém. Inst. fond. Afr. noire 84: 401-402. 


1969b. Philosycus, a new genus of fig wasps allied to Otitesella Westwood 
(Hymenoptera Chalcidoidea, Torymidae).— Ann. Mus. R. Afr. centr., in 8, Zool. 175: 
439-445. 

1969c. Hymenoptera Agaonidae, with an introductory chapter on West African 
fig wasps.— Ibid. 175: 449-464. 

1970a. Revision of the Agaonidae described by J. Risbec, and notes on their 
Torymid symbionts (Hymenoptera, Chalcidoidea).— Zool. Meded., Leiden 45: 1-16. 

1970b. Vijgen en vijgewespen.— In K. H. Voous (Ed.), Biosystematiek: 180-206. 
240-242. 

1971. A new record of Allotriozoon prodigiosum Grandi, and description of 
its symbionts (Hymenoptera, Chalcidoidea).— Mém. Inst. fond. Afr. noire 86: 367-383. 

1972a. A new species of Agaon from Nigeria (Hymenoptera, Chalcidoidea).— 
Ent. Ber., Amst. 32: 122-124. 

1972b. The genus Alfonsiella Waterston (Hymenoptera, Chalcidoidea, 
Agaonidae).— Zool. Meded., Leiden 47: 321-330. 

1973. Phylogenetic specificity of figs and fig wasps——Jn N.B.M. Branjes (Ed.), 
Pollination and dispersal: 21-25. 

1974a. Nigeriella, a new genus of West African fig wasps allied to Elisabethiella 
Grandi (Hymenoptera Chalcidoidea, Agaonidae).— Zool. Meded., Leiden 48: 29-42. 

1974b. The fig wasp genus Diaziella Grandi (Hymenoptera Chalcidoidea, 
Torymidae Sycoecini)— Proc. Acad. Sci. Amst. (C) 77: 295-300. 

1974c. Species of Agaon Dalman and Allotriozoon Grandi from Africa and 
Malagasy (Hymenoptera Chalcidoidea, Agaonidae).— Zool. Meded., Leiden 48: 123-143. 

1974d. Philippine fig wasps 1. Records and descriptions of Otitesellini 
(Hymenoptera Chalcidoidea, Torymidae).— Ibid. 48: 145-161. 

1975. Fig insects from Aldabra (Hymenoptera, Chalcidoidea)— Ibid. 49: 
225-236. 

1976. Indo-Malayan and Papuan fig wasps (Hymenoptera, Chalcidoidea) 7. 
Agaonidae, mainly caught at light— In preparation. 


The Taxonomist’s Dilemma 


by 
V. H. HEYWOOD 


Department of Botany, Plant Science Laboratories 
University of Reading, England. 


Taxonomists, or at least the services they provide, are suddenly in demand. 
This is not quite the same as saying that taxonomy has regained its earlier 
popularity — indeed there are signs that in some of the developed countries the 
number of students going on to seek taxonomic training is decreasing after reaching 
a peak in the 1960’s. Teaching and research schools are in some cases being run 
down and in some major European universities they are non-existent. Likewise 
many important museums and herbaria are understaffed and the accumulation of 
unidentified material is often of massive proportions. 


The pressure for an increase in the number of taxonomists stems largely from 
the growing and realistic appreciation of both the extent and pace at which man has 
been consuming, destroying, modifying and deteriorating our global environment, 
and in particular our plant resources which form the very base of the life-support 
systems of our planet (Heslop-Harrison, 1975), and from the initiatives that have 
been proposed to combat this. The most important recognition of the dangers 
facing plant life, and of the consequences for man if urgent steps are not taken to 
moderate them, comes from the United Nations Conference on the Human Environ- 
ment held in Stockholm in 1972 and the ensuing recommendations 39-45 of the 
Declaration on the Human Environment dealing with plant and animal resources, 
their survey and conservation. If one considers the main recommendations, they 
cover survey of plant genetic resources, preparation of inventories, field exploration 
and collecting, conservation in nature and in gardens and seed banks. To those of 
us who work as practising taxonomists this sounds all too familiar, since it is a 
fair summary of the kinds of activities in which we and previous generations of 
taxonomists have been engaged for the past two centuries. What does the taxonomist 
do if not explore plant resources in the field throughout the world and produce 
checklists, Floras, keys and monographs, which are essentially inventories with 
a greater or lesser amount of detail? Yet the role of taxonomy is not explicitly 
recognized. Conservation, resources, ecology have become accepted words, even 
today understood by governments, but taxonomy still does not have a familiar 
ring and the term classification still retains a pejorative gloss. A similar failure 
to appreciate the role of taxonomy was a characteristic of the International 
Biological Programme, yet the evidence of the urgent need to extend floristic 
exploration, especially in areas at high risk such as the tropics, sub-tropics, islands 
and areas of Mediterranean climate, was fully available. Among those to draw 
attention to the need to study the tropical floras, Corner was prominent as early 
as 1946. His appointment to a professorship of Tropical Botany by the University 
of Cambridge was a belated recognition of both the importance of his work and 
his personal standing, but his pleas for action went largely unheard by governments 
and international agencies. 


_ Explicit recognition of the need for an expansion of taxonomic work was 
given at the 18th General Assembly of the International Union of Biological 
Sciences in 1973, which passed resolutions recommending that special attention be 


233 


234 Gardens’ Bulletin, Singapore — XX1X (1976) 


given to the improvement of the services providing for the identification of animal 
and plant species, as well as to the improvement of the flow of information on 
taxonomic data to all other relevant disciplines, and requesting that the Executive 
Committee point out to the national adhering organizations the great importance 
of the training of biological taxonomists. Similar resolutions have been passed by 
congresses and symposia but it would be unrealistic to expect any substantial action 
to be taken by governments especially in the present economic climate. The 
problems of supply and training of taxonomists have already been alluded to 
briefly and will be discussed further below. 


It is against the above background that taxonomists work today; not a 
particularly comforting one. It contrasts with previous generations of taxonomists 
who worked with a high degree of tranquillity, not faced with an agonizing series 
of choices of techniques, priorities, philosophies. 


In the post-Linnean period, as the exploration of new territories in various 
parts of the world gathered momentum and material flowed into botanic gardens, 
herbaria and museums, taxonomy rapidly progressed from being essentially a 
codification of folk biologies, and mainly West European, to a world-wide system 
of classification and communication for biology. The fact that this fundamental 
change in the nature of taxonomy had taken place was scarcely realized at the 
time (Heywood, 1974). Indeed one of the unfortunate consequences of the 
acceptance of Darwinian evolutionary theory was that attention was diverted 
from the practical data-processing role of taxonomy to an almost obsessive com- 
pulsion to seek evolutionary interpretations of taxonomic data and to place all 
organisms in their correct place on so-called phylogenetic trees. This preoccupation 
with evolutionary explanation has, quite understandably, continued to the present 
day: in the age of evolutionary biology it could scarcely be otherwise. What has 
seldom been assessed is what the effect on practical classification has been. To the 
extent that comparative data have been deliberately discarded or ignored in 
favour of supposedly phylogenetically significant features, and thereby departing 
from the principles of classification based on maximum co-variation or correlation 
of characters, it is arguable that taxonomy has been greatly retarded. This, 
combined with the tendency to decry the importance of taxonomy as an information 
system, may well have set classificatory taxonomy back ten or twenty years. Today 
when we have powerful tools for the study of phylogeny, such as numerical 
cladistics, and powerful new classes of data, such as amino acid sequences of 
cytochromes c and plastocyanins, we are in a situation where we have to consider 
seriously whether we can afford to devote a major effort to this kind of study, or 
whether we should concentrate our energies and resources on floristic exploration 
and writing Floras and monographs. Similarly we must ask whether detailed 
study of micro-characters by scanning electron microscopy, chemical features by 
gel electrophoresis, chromatography, etc., or the population structure of temperate 
species of no known or potential economic, ecological or agronomic importance, 
can be justified. 


To answer that we must continue to do both is to sidestep the dilemma that 
faces us today. What then has happened that has forced us into this situation? 
Quite simply, our predecessors, after earlier naive assumptions as to the numbers 
of the world’s biota, came to realize that the task facing them in exploring, 
describing and understanding the world’s flora and fauna was virtually limitless, 
but that it would only be a matter of time before the basic inventorying would be 
complete. The great museums and herbaria were established and collections were — 
amassed from region after region as part of an apparently never-ending process. For _ 
political-historical reasons, floristic exploration and Flora-writing was a feature 
associated with imperialism and colonialism as regards the under-developed, — 
largely tropical, parts of the world and no global assessment of progress was 
ever seriously made. | 


The Taxonomist’s Dilemma 235 


It is only in the course of the last five to ten years that we have come to 
realize that the end is in sight and that we have achieved much less than we had 
realized. This new situation has arisen because of expanding world populations 
and increased expectations as regards living standards, with all the consequent 
destruction of natural vegetation, especially tropical forest, which is basically 
non-renewable, for living room, cultivation, industrialization, etc. The statistics 
are horrifying and sufficiently well documented to need no repetition here. The 
almost inevitable outcome will be massive world-wide extinction of the world’s 
most interesting and economically valuable floras and their replacement, where 
there is space still available by some form of secondary and relatively uniform 
vegetation. 


The probability that about 85% of the world’s extant organisms have not 
yet been described need not concern us here: there never was any possibility that 
they would or even should all ever be discovered and named. The position 
concerning higher plants is on the face of it much more satisfactory — it is 
estimated that about 250,000 species of angiosperms have been recognised and that 
only 10-20,000 still remain to be discovered and described. Unfortunately we 
know very little about the great majority of the quarter million species apart 
from some of their basic morphology and some distributional and ecological data. 
For only a tiny minority do we possess details of their karyology, population 
structure, chemical constituents, breeding system, etc. 


What makes the situation so serious is not the eventual outcome but the 
alarmingly rapid rate at which species by the hundred and thousands and indeed 
whole ecosystems, are either disappearing or becoming threatened. While we can 
make estimates such as those which suggest that up to 20,000 angiosperm species 
are threatened or even in danger of extinction, our impotence is triple in that (1) 
the majority are in tropical or sub-tropical areas of the world, (2) we do not have 
the means of taking action on a sufficiently massive scale to avoid the inevitable 
extinction of a high percentage of them due to lack of funds and trained man- 
power, not to mention sociological and political factors, and (3) we have no 
means of knowing, even were the resources available to tackle the problem, exactly 
which species are in greatest peril. 


Despite the valiant efforts of the IUCN and its Threatened Plants Committee 
to identify and catalogue the threatened species. It is only in cool temperate and 
perhaps Mediterranean regions where this will be achieved in time. 


The immensity of the problem in the tropics is such that the action needed is 
vastly in excess of the manpower and resources available or likely to become 
available in the near future and we can only hope that a sufficient number of 
national parks and reserves can be established and maintained so as to allow 
us to retain for future generations some reasonably representative samples of the 
floristic richness and resources of the various countries and regions concerned. In 
addition to such natural reserves, it is necessary to establish seed banks and living 
resources centres, especially in scientifically organized Botanic Gardens as discussed 
at the Kew Conference held in September 1975 sponsored by the NATO Eco- 
Sciences Panel. Such action is already being organized by various international 
agencies for cultivated plants and their wild relatives, which is a big enough task 
in itself, but it must be extended to deal with at least some of the wild species 
to which no economic importance is at present attached. Just how such species 
should be selected is a major problem since, as indicated above, our detailed 
knowledge of large parts of tropical floras is so limited that we cannot in many 
cases say which of them are threatened. 


In the light of the situation a positive response is needed from the taxonomic 
community, yet all too often the reaction is either that the problem is so vast 
that nothing any individual taxonomist can do will have any effect, or that the 
whole question is one for politicians, economists, and governments, not scientists. 


236 Gardens’ Bulletin, Singapore — XX1X (1976) 


I believe that this is unduly pessimistic an attitude to take. The taxonomist 
is often uniquely qualified to know what the situation is in a particular area and a 
great deal could be done by devoting effort to identifying areas or species at high 
risk and further by assembling this information for general use. One urgent task 
is to make a world survey, country by country of the floristic situation — what the 
size of the flora is, how far it has been studied, what Floras are available, are in 
preparation or are being planned, what the manpower situation is, which countries 
are involved, what assistance is needed. Surveys of this kind have been undertaken 
for Europe through the Flora Europaea organization, for the Mediterranean 
through the CNRS symposium on the Mediterranean basin held in Montpellier 
in June 1973 and through a working party of the OPTIMA organization and for 
all Africa south of the Sahara by AETFAT. 


There is a widespread feeling amongst taxonomists that they should have 
freedom to work on any group no matter what the overall situation might be. 
At the risk of being highly unpopular, I feel that such an attitude is today 
somewhat arrogant, especially when one considers that most taxonomists are 
employed from public funds. Very few scientists today have such freedom of choice 
and I believe that taxonomists today should seriously consider whether there is 
not some positive action they could take to help in a small way to alleviate the 
situation outlined above. It is easy enough to append signatures to resolutions and 
to lament the perils facing the world’s flora but this is hypocritical if at the same 
time research programmes are undertaken without regard to these considerations. 
It would not be difficult to compile a list of taxonomic groups deserving high 
priority either because they contain many threatened species or because they are 
of economic importance, and have not been adequately studied or revised. Closer 
collaboration, for example, between taxonomists and agronomists and plant 
breeders should be urged in areas such as exploration of genetic resources, 
collecting material for seed banks and living collections. 


There are two further areas which should make claims on our time — 
education and training. Our first concern should be to try and educate our colleagues 
by explaining patiently the need for what seems to them quite routine and 
unspectacular research. To a large extent our own insistence that we are all 
evolutionary biologists concerned with the solution of what to the outsider may 
seem quite parochial problems has been largely responsible for our failure to 
convince our colleagues of the seriousness of the threats facing plant resources 
today. However intellectually stimulating the search for evolutionary ancestors 
may be, it has diverted attention from the real-life situation. For too long, 
conservation has been left in the care of the prophets of doom, rather than 
accepting our own responsibilities to present the hard facts in a realistic way. 
If we, as taxonomists, with our own intimate knowledge cannot get the message 
across, then who will? 


Training of taxonomists prevents a whole series of problems. Those of us 
with the facilities and staffing have a moral responsibility to accept the rdle of 
training, as best we can, taxonomists for those countries where qualified staff are 
distinguished by their scarcity. Our aim should be to train the teachers so that 
they can take over the tasks in their own land. At the same time we should resist 
attempts by government to restrict our rdle in this area because of temporary 
economic difficulties. 


Finally we should draw attention to the consequences if we do not take — 
action on a large enough scale. It is not just the tropical countries but the whole | 
of mankind that will suffer if we are to do too little, too late. We have a respon- 
sibility not only to ourselves but to future generations. rs 

Professor Corner was one of the first to draw attention to the taxonomist’s 
dilemma. If we have any criticism to make it is that he did not from his wisdom 
plead the case with even greater eloquence than he did. 


The Taxonomist’s Dilemma 237 


References 


HESLOP-HARRISON, J. 1975. Man and the endangered plant. Jnternational 
Year Book 1975: xXii-xvi. 


HEYWOOD, V. H. 1974. Systematics — the stone of Sisyphus. Biol. J. Linn. Soc. 
6: 169-178. 


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hen unigdery cusiied fo ROW wht ‘ist it dation 
sonata sala barosnebna’ orl), bees fiat 

ine eefce cation for: 


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dee vibra 

Th. We Det: 


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as tod rs ~ af, o, oe he mia i i) ¥ on ae q 
Gh igankteed twat whe 2 eter’ hi: » Sea 
sists Satie Giaky tor Cagepih ee hive, ge 
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eet 


On the Style of Floras: some general considerations* 


by 
D. G. FRODIN 


Herbarium 


University of Papua New Guinea 


Summary 


The most satisfactory style for a Flora at the present time should be one of conciseness 
and practicality, with “correctness and clearness of method and language [being] the first 
qualities requisite,” to quote Bentham (1874, p. 50). This should be inventory, identification, 
and provision of essential data. Large-scale flora projects, of which there are perhaps too 
many on the stage today, should be examined very carefully; in many cases their bulk (and 
cost) may defeat any real usefulness or impact, and their basis is shaky, leaving many to 
be terminated incomplete or only completed after more than a generation. Such incomplete 
works, with which the pages of floristic bibliographies are replete, are ultimately of Icss 
value than one which may be more modest but is complete, and in fact should perhaps 
a viewed as a wasting of botanists’ time and resources. Furthermore, with the EDP-IR 
communications, and media revolutions (the full impact of which has yet to be felt in 
systematic biology), it may be questioned whether much of the specialized data found in 
large-scale floras need be tied up in the print medium but could better be handled in other, 
less familiar ways; at the same time, such methods would lead to fewer losses than is 
usually the case at present in translating taxonomic and floristic research into conventional 
floras. The FNA represented a step in the right direction, but it faced public relations 
problems and an unfavourable administrative climate and it may have been too big a step 
at that time and place. Some smaller but similar projects are still under way in other parts 
of the world and it is these “guinea-pigs” that will be watched with interest in the next 
few years. However, there is still plenty of scope for the more modest, concise work, which, 
because less time is usually taken in production, stands a better chance in the present economic 
climate of gaining support and carrying through to completion, although technically it might be 
less “prestigious”. It is thus to be hoped that works such as Flora Europaea, Flora of Turkey, 
Flora Iranica, and the Tree Flora of Malaya will be successfully completed in the next 
decade, and others like them undertaken, even for lesser-known tropical regions. There is 
also, in my view, scope for good annotated enumerations, preferably with keys; the recent 
Prodromus einer Flora von Siidwestafrika is a good example. 


The completion of a revised and expanded version of my Guide to standard 
floras of the world, which first appeared in a limited cyclostyled edition in 1964, 
has provided the opportunity to make a review of the purpose, design, and content 
of floras, manuals and enumerations; additional stimulus for this has come from 
a series of recent articles dealing with various aspects of the subject (Fisher, 1968; 
Heywood, 1973; Shetler, 1971; Taylor, 1971; Watson, 1971). These in turn resulted 
from a consideration of the “information explosion” in systematics (see also Anony- 
mous 1974), the introduction of the new methodologies of taximetrics (numerical 
taxonomy) and EDP-IR during the 1960’s and early 1970’s, the progress of Flora 
Europaea, the development of the Flora North America Program (before its 
termination in 1973), and the increasing demands on the systematics profession 
made by other biologists (notably ecologists) and by “‘environmental scientists.” 
Together, these papers represent the first major reconsideration of the principles 
and the style of floras and other floristic works for a century or more, with a few 
exceptions (van Steenis, 1954; Davis & Heywood, 1963). The present review gives 


* This essay was originally intended to be one of the introductory chapters to my forth- 
coming Guide to standard Floras of the world, but had to be omitted for lack of space. 
It is presented here as a separate work. 


239 


240 Gardens’ Bulletin, Singapore — X XIX (1976) 


a summary of these contributions and traces the historical development of Flora- 
writing as well as analyzing current trends and making some suggestions for the 
future. 


HISTORICAL SURVEY 


Most of the more important floristic works in current use around the world 
by and large adhere to principles gradually laid down in the mid-19th century 
and succinctly summarized by Bentham (1861, 1874) and de Candolle (1880). 
Bentham’s principles are contained in the first five aphorisms of his ‘“‘Outlines of 
Botany”, which appeared in nearly all of the colonial floras in the series issued 
from the Royal Botanic Gardens, Kew, as well as some contemporary works such 
as Hillebrand’s Flora of the Hawaiian Islands. Their influence was widespread 
and lasting, and because the first three are particularly apropos to the present 
discussion I repeat them here: 


“1. The principal object of a Flora of a country, is to afford the 
means of determining (i.e. ascertaining the name of) any plant growing 
in it, whether for the purpose of ulterior study or of intellectual exercise. 


2. With this view, a Flora consists of descriptions of all the wild or 
native plants contained in the country in question, so drawn up and 
arranged that the student may identify with the corresponding description 
any individual specimen which he may so gather. 


3. These descriptions should be clear, concise, accurate, and 
characteristic, so as that each one should be readily adapted to the plant 
it relates to, and to no other one; they should be as nearly as possible 
arranged under natural divisions, so as to facilitate the comparison of each 
plant with those nearest allied to it; and they should be accompanied by 
an artificial key or index, by means of which the student may be guided 
step by step in the observation of such peculiarities or characters in his 
plant, as may lead him, with the least delay, to the individual description 
belonging to it.” 


The second part of the fifth aphorism is also of some interest and is likewise 
quoted: 


“The botanist’s endeavours should always be, on the one hand, to 
make as near an approach to precision as circumstances will allow, and, 
on the other hand, to avoid that prolixity of detail and overloading with 
technical terms which tends rather to confusion than clearness, In this he 
will be more or less successful. The aptness of a botanical description, like 
the beauty of a work of imagination, will always vary with the style and 
genius of the author.” 


The first of these aphorisms clearly reflects Bentham’s view of a flora; 
and it was in this spirit that much of the “Kew Series” of colonial floras 
was prepared, as with the contemporary floras of the British Isles prepared 
by him and by Hooker (these latter, even today, are still appreciated for their 
method and conciseness). Bentham’s principles, with modifications, also gave rise — 
through the example of Torrey’s and Gray’s classic works on North American — 
plants of the late 1830’s and 1840’s to the standard format of many current North © 
American Floras and manuals. Other major works of the period strongly influenced — 
by these principles — as acknowledged by their authors — were Miquel’s Flora — 
indiae batavae (1855-59), Boissier’s Flora orientalis (1867-88), and Willkomm & 
Lange’s Prodromus florae hispaniae (1861-93). 

In kindred spirit to the concisely descriptive floras of the Anglo-American 
(and Franco-Swiss) “‘school”, but with somewhat different methodology and aims, 
there arose the Continental ‘“‘manual-key”. This represented a _ substantially 


Style of Floras 241 


independent development, stemming from the simple dichotomous analytical keys 
devised by Lamarck for the first edition of his Flore francaise in 1778 (Voss, 1952; 
quoted in Radford et al., 1974). Lamarck intended this work to be nothing more 
than a handy means of plant identification (Stafleu, 1971), and all manual-keys 
which have appeared since then have been motivated by this principle. In such 
works, the format of separate keys (or synoptic devices) and descriptions typical 
of works of the Anglo-American “school”? was bypassed in favour of diagnostic 
analytical keys which (in later years) also variously incorporated brief, partly 
symbolic notes on habitat, distribution, life-form, phenology, karyotypes, etc. As 
the 19th century progressed, bringing with it greatly improved means of transporta- 
tion and more leisure, the manual-key style became very widespread in Europe, 
often going under the name of “excursion-flora.”” Through Central European 
influence, this kind of flora penetrated to Russia and eventually became an 
ubiquitous feature in the comprehensive network of regional floras which developed 
in the Soviet Union from the 1920’s onwards. (The Russian term for such works 
is opredelitel’, sometimes translated as “‘the keys” or “‘determinator” but better 
rendered in English, I feel, as “‘manual-key”, being more expressive and _ idio- 
matic.) However, no matter where they are produced, manual-keys are to a large 
extent based on more comprehensive “‘research’’ or “‘creative’’ floras; because of 
their largely derivative nature and (in some parts of the world) periodic issue to 
meet public demand, they (along with local descriptive manuals) have been termed 
“routine” floras (van Steenis, 1954; Davis & Heywood, 1963). As a style, the 
manual-key is not often seen outside Europe of the Soviet Union; good recent 
examples by non-Continental authors include Flora of the Sydney Region by Beadle 
et al. (2nd ed., 1972) and Flora of the Pacific Northwest; an illustrated manual by 
Hitchcock and Cronquist (1973). 


An interesting link between the two “schools” was provided by the floras 
written by Bentham (and those influenced by him). Although these works were 
basically concisely descriptive. like most of those written by the de Candolles, the 
Hookers, Torrey and Gray, Bentham consistently used analytical keys in place of 
(or in addition to) the synoptical devices which characterized the works of the 
other authors (and those influenced by them). This reflects the strong influence 
of the Flore francaise of Lamarck (by 1815 under de Candolle’s authorship), with 
its analytical keys (or ‘‘indexes’’, to use Bentham’s term), and other French works 
during Bentham’s formative years as a botanist (1817-26), which were spent in 
France (Bentham, 1974). By contrast, J. D. Hooker apparently believed that such 
keys made things too easy in that students would pay little attention to diagnoses 
and descriptions. This view may well have been shared by A. de Candolle, who 
failed to mention them in his La Phytographie of 1880 (van Steenis, 1954). 


The next major development in floristic writing to be considered here is the 
detailed semi-monographic flora, which also had its origins in the mid-19th century. 
It seems likely that the motivating forces for such works were prestige (something 
which also lay behind the many sumptuous sets of “‘scientific results” of voyages 
and expeditions in this period) and a belief that a flora should act as a detailed 
compendium and repository of information about the plants of an area and not 
solely as a practical handbook for identification and essential information. In other 
words, it should be a specialized kind of encyclopaedia, with sub-monographic 
accounts containing detailed descriptions, synonymy, specimen citations, extensive 
notes, and (often) illustrations in large plates. This concept of a flora seems to 
have arisen (or taken strongest hold) in the Central European intellectual sphere, 
and cannot fail to have been influenced by the Germanic prediliction for detail 
rather than conciseness, It was here that the Linnean system persisted longest, due 
largely to the strength of the scholastic tradition (and the ex cathedra professorial 
System) and the continuing demand for general compendia of the plant kingdom 
(Bentham, 1874). The first truly original systematic work in Central Europe which 


242 Gardens’ Bulletin, Singapore — XX1X (1976) 


professed a “‘natural’’ system was Endlicher’s Genera plantarum (1836-40). Soon 
after, Endlicher joined forces with von Martius to work on the first “modern” 
semi-monographic flora, the king-sized Flora brasiliensis, begun in 1840. In this 
way, the endemic mania for large compendia was shifted into significant new 
channels, the results of which were to have a major influence over the next two 
generations. 


The greatest flora of the 19th century dragged its detailed pages slowly on for 
66 years, a time span exceeding that of most British colonial floras of the same 
period, and was for long a dominant factor in European phytography. As with 
Flora Europaea a century later, its organization consisted of editors, technical 
co-workers (‘‘Privatassistenten’’), and numerous specialist contributors, Amongst 
the many botanists so involved, there were three — Eichler, Engler, and Urban — 
who brought the Berlin “‘school”’ of systematics into being after 1870 and imbued 
it with the Weltanschauung and scholarship which were to make it so influential. 
All had been, or were actively, editors or co-workers or both on Flora brasiliensis. 
Under the general direction of Engler after 1889, the Berlin “‘school’”’ came to 
specialize in large-scale monographic works, detailed series of regional revisions, 
plant-geographical studies, and related contributions, culminating in that supreme 
monument of German systematics, Die natiirlichen Pflanzenfamilien (1887-1915; 
2nd ed., 1926+, not completed). Contemporaneously with much of Flora brasi- 
liensis, but on the domestic front, there was another large-scale work, the 
Reichenbachs’ Icones florae germanicae (1834-70). 


In spite of all this effort, and the stimulus provided by the development of 
the German colonial empire after 1880, few, if any, concise practical works ever 
appeared; there was nothing comparable to the “Kew Series” or the range of 
regional manuals in North America. Indeed, the influence of the Berlin school 
under Engler led to a very widespread emphasis on synthetic work, and less 
attention was paid to floras in the late 19th and early 20th centuries, at least in 
Europe (Davis & Heywood, l.c., p. 33.) One example of a German colonial flora 
is Schumann and Lauterbach’s Die Flora der deutschen Schutzgebiete in der 
Stidsee (1900-05) for German New Guinea, Micronesia, and Samoa. This is 
essentially an enumeration, containing a useful repository of geographical and 
other data but lacking in methodical organization and largely innocent of keys. It 
is all but useless for identification and cannot be compared with a work such as 
Merrill’s Flora of Manila (1912). Perhaps, indeed, the Central European predilic- 
tion for detail was of such a nature as to have precluded (or retarded) the 
development of a practical philosophy towards floras, at least outside Central 
Europe and its many “‘excursion-floras.”’ Writing in 1874 of German botany, 
Bentham remarked, ‘““The country abounds in those plodding minds which revel 
in the working out of minutiae of detail, and, to find their way, are satisfied with 
a sexual, alphabetical, or any other artificial index ...” A similar lack of method 
also marred much of von Mueller’s writings on the Australian and New Guinean 
floras, and the same could be said of some Dutch works on the East Indies. In 
France, no characteristic “‘school’”’ developed apart from the influences of Lamarck 
and the de Candolles and, indeed, few important floras appeared under French 
auspices in the mid- and late 19th century. The suppression of any chair at the 
Sorbonne or the Paris Museum specifically responsible for systematics and classi- 
fication between 1853-73 and the associated loss of the Delessert Herbarium to — 
Geneva in 1869 were serious setbacks (Leandri, 1967) and present French activity i 
in the writing of floras is largely a development of the 20th century and one 
showing few original features. Lf 

The final key development in floristic writing to be considered here was the 
annotated enumeration or checklist. These began to appear from the late 19th 
century onwards as an outgrowth of the “synopsis” or “‘systema vegetabilium”, 
and are essentially catalogues. Generally they were viewed as an interim measure, 
so that something of the results of floristic research could be made available to the 


Style of Floras 243 


public in a concise, easily prepared form, or as works in which much descriptive 
detail was considered unnecessary, such as local or insular florulas, While the 
majority of such works cover relatively small areas, there have also been produced 
a goodly number of extensive annotated enumerations for large, often botanically 
poorly known areas, especially in the tropics. Notable examples of large enumera- 
tions include Enumeration of Philippine flowering plants (Merrill, 1923-26); 
Conspectus florae angolensis (Carrisso et al., 1937+ ); Enumeratio spermato- 
phytarum aethopicum (Cufodontis, 1953-72); and Catalogus florae domingensis 
(Moscoso, 1943). Many of the authors/editors lacked the means and/or time to 
prepare full descriptive works but believed some kind of consolidated publication, 
even if imperfect, was necessary. While they have been criticized by some writers, 
such works should be regarded as better than no consolidated work at all, and in 
many cases have fared, or may fare, better than semi-monographic floras. 

The preferred contents of floristic works have been well summarized for our 
time by Blake and Atwood (1942, p. 8-9) and Davis and Heywood (l.c.) and need 
not be reiterated here. The question of content has also been considered by van 
Steenis (1954) and Brenan (1963). The most important additions and refinements 
to the standardized formats of Flora-writing have been in the areas of nomenclature, 
ecology, chorology and distribution, mapping, karyology, critical commentary, and 
illustration, The findings of palynology and comparative phytochemistry have left 
their imprint largely above the species level. In general, it may perhaps be said 
that standards with regard to content have gradually improved in the years since 
World War II. 

On the other hand, the present century has by and large witnessed a con- 
comitant — and perhaps inevitable — increase in the bulk (and cost!) of Floras 
and, often, a decrease in utility. There has perhaps also been a tendency in many 
cases not to think out clearly the aims and purpose of a given floristic project. Such 
trends have been deplored by van Steenis (/.c.) who believed that ‘“‘recent Floras 
often differ considerably from Bentham’s scheme’’. Davis and Heywood (l.c.) 
further note that there are a number of works called “‘Flora”’ which contain keys 
but no descriptions, as well as some with descriptions but no keys; instances of such 
works still may be found amongst even very recent floristic literature. Some floras 
contain an exceptional amount of non-phytographic matter and must be viewed 
more as encyclopaedias than as practical manuals. In this connexion, it is interesting 
to note that very few writers after 1880 (and until recent years) appear to have 
seriously reconsidered the philosophy and methodology of floras, despite their great 
importance as a means of phytographic communication (van Steenis, /.c.; Heywood. 
1973). Perhaps, as van Steenis notes, the older writers (especially Bentham) “‘had 
at the time exhausted the subject in such an admirable way that nobody found 
occasion to discuss it any further.” He noted that Diels in his Methoden der 
Phytographie of 1923 did not give special attention to this question — a curious 
Omission in view of the large contributions to floristic literature by German and 
Central European botanists but perhaps explicable in view of the relative lack of 
concern with method and conciseness in so many of these works. 


Since World War I, and even more so since the last war, there has been a 
distinct tendency towards the creation of large-scale, multi-author flora series for 
many countries or regions where knowledge of the plant life is imperfect in one 
way or another, particularly in the tropics. In addition, with an increasing amount 
of material to be covered as well as increasing specialization, more and more of 
the larger floras have been issued in serial parts, without regard to systematic 
order. Some of these become partial substitutes for serious monographs, for which 
there seem today to be few satisfactory publication outlets and which in some 
quarters appear to have a low academic “‘status” (cf. Jacobs, 1969). In many 
botanical circles today, it seems that large-scale floristic projects have become 


244 Gardens’ Bulletin, Singapore — X XIX (1976) 


“fashionable”, the rise and fall of the Flora North America Program notwith- 
standing, and the resulting floras have a certain “prestige” value. A number of 
these have been set up for smaller, mostly politically delimited units (mainly 
within the tropics), despite the advice of van Steenis who believed that large-scale 
‘“‘creative” floras should be written with reference to large, natural botanical 
regions such as Malesia. Most larger botanical institutes in North America, Europe, 
and (to a lesser extent) elsewhere presently have one or more of these pro- 
jects under way. Some of these works are meaningful, and as they progress 
represent real contributions to knowledge, although perhaps in some cases pro- 
gressing too slowly; examples include Flora Malesiana, Flora Iranica, Flora 
Neotropica, Flora SSSR, and some of the African floras. Others are too detailed 
or otherwise long-winded, too grandiose, cover unnecessarily small areas, or have 
an insecure basis. The length of time taken, or likely to be taken, to complete 
many of these works is quite considerable; this in itself raises questions about 
financing as well as individual and institutional motivation (de Wolf, 1963, 1964). 
The time-span of Flora brasiliensis has already been mentioned; other examples 
are the Flora of Peru (40 years, still incomplete and interest fading); Flora 
capensis (74 years, with a 3l-year break from 1865 to 1896); Flora of Tropical 
East Africa (23 years and quite some way from completion); Flora Polska (56 
years, although all but complete); Flora SSSR (30 years); and Flora Malesiana 
(27 years, only some 30-40% completed, and some families unlikely to be 
published). For these and other reasons, De Wolf has questioned the wisdom of 
many large-scale projects, suggesting instead that more attention be paid to the 
preparation of ‘“‘concise” works (although the objection would be raised that for 
many little-known regions, a substantial amount of basic monographic and 
revisionary work is required in connection with a flora project and this must be 
expressed in some way in the published flora, because there may be no alternative). 
Fortunately, some over-elaborate works have been discontinued; a notable example 
is Genera et species plantarum argentinarum (1943-56). I consider, however, that 
the whole question of large-scale floras should be looked at more closely, with a 
view to making further cuts and consolidations and storing a considerable per- 
centage of data outside the print medium (or at least outside the realm of the 
standard flora). 


FLORAS AT THE PRESENT TIME 


At the beginning of this paper, I noted that in recent years there has been 
an information explosion in systematics, from which Floras have not been spared. 
The impact of this, together with the introduction of EDP-IR methods, has led to 
considerable recent discussion of the content and style of floras and the philosophy 
and methodology of flora-writing —- the first substantial debate for some 100 years 
in this area, with only very few key contributions in the intervening period. As this 
is very much a current issue, which Heywood (1973) believes to be of “‘crisis” 
proportions, it seems useful to consider the progress and problems of Flora-writing 
at the present time and to make some suggestions about the future, with particular 
reference to infra-tropical regions. 


The continued acceptance — perhaps uncritically — of long-standing and 
stereotyped formats and sets of questions for floras and related works by genera- 
tions of botanists is not only evidence of their general utility but also a reflection 
of the conservatism inherent in much of the taxonomic profession; in other words, 
tradition has perhaps been as strong a force as any intrinsic merit in these 


parameters, Taylor (1971) states that these are some 200 years old but as I have | 


shown in this paper the design principles and content of most present-day — 
descriptive works are largely based on principles laid down between 1830 and 1860 _ 


(with manual keys and enumerations (or catalogues), as well as ligneous Floras, 
evolving later to meet particular needs or to cope with difficult situations like the __ 


inventorying and classification of Floras of humid tropical regions). 


Style of Floras 245 


An examination of the relevant literature cited at the beginning of this paper 
as well as personal observations suggest that at present there are essentially two 
views, both of long standing and to some extent at odds, concerning the central 
purpose of descriptive floras. This, in some way, parallels van Steenis’s view that 
most floras are ‘“‘dualistic’’ in nature, i.e. they attempt to serve two different ends, 
the one archival or encyclopaedic, the other for identification (van Steenis, 1962). 
He argued that this problem could be resolved in north temperate regions, but not 
in the tropics. A similar theme has been central to the current ongoing discussion. 


The first philosophy — one which sees Floras as tools for identification — harks 
tight back to the first aphorism of Bentham quoted early in this paper. The 
relative value of this philosophy has again been emphasized by Heywood (1973) 
as well as indirectly by Watson (1971). Heywood suggests that Floras should 
address themselves to the following questions about the plants of an area: 


(a) what there is, 
(b) how they may be recognized, and 
(c) where they may be found 


and that this involves keys, descriptions, auxiliary data, and necessary nomen- 
clatural apparatus. It is argued that Floras were not necessarily intended to serve 
as sources of strictly comparative data. This philosophy is in general also adhered 
to by Brenan (1963) in his review of the role of Floras in developing countries. 


The second philosophy — in which floras are seen as essentially archival or 
encyclopaedic — has its roots in the Flora brasiliensis tradition, is exemplified in 
many large-scale flora projects today, and considers that floras should be “a 
physical repository of descriptive data about plants which are organized and 
formatted, usually in book form, so as to answer to time-tested set of prescribed 
questions ...”’ (Shetler, 1971). 


The differences between these two philosophies as related to developments in 
the 19th century have already been discussed, with several examples. In our own 
day, the first philosophy is well exemplified by Flora Europaea, which will ultima- 
tely deal with some 15,000 species in five quarto volumes. Other examples of recent 
floras where an attempt has been made at conciseness are Flora iranica, Flora of 
Turkey, Flowering plants of Jamaica, Prodromus einer Flora von Stidwestafrika, 
and Flora of West Tropical Africa (2nd ed.) as well as many smaller descriptive 
floras and manuals. 


In this connexion, it may be noted that the longest time that will have been 
taken for these projects is about 25 years (Flora Europaea), something hardly ever 
achieved by most of present-day large-scale flora projects, which in most cases 
will take anywhere from 20 to 40 or more years to complete (cf. De Wolf, 1963). 
In addition, the creation of large-scale works, involving lengthy research and pre- 
paration and sometimes interinstitutional cooperation, involves a considerably 
greater investment of time and manpower (averaging 50 species per year per 
taxonomist) as opposed to the production of “‘concise’ works (averaging 250 
species per year per taxonomist) (De Wolf, 1964). 


Sometimes the two philosophies are confused. In the “Introductory Notes” to 
the Flora of Papua New Guinea Concise Handbook Project (of which nothing 
has yet been published) it is stated that, in order to make available “information” 
on the flora (which is presently very scattered apart from what is available in 
Flora Malesiana), the sponsoring institutions have “‘embarked on a project to 
produce, in a handbook format, a concise Flora ...” By contrast, the one sample 
family treatment seen suggests that the work, even with some information pre- 
viously relegated to “technical supporting papers’’, will be somewhat encyclo- 
paedic in nature; four pages of text are required to deal with three species. This 
is hardly “‘concise” in the sense of the Benthamian tradition or the Flora of Turkey 


246 Gardens’ Bulletin, Singapore — XX1X (1976) 


but more like the Flora of Guatemala or even Flora Malesiana — both essentially 
large-scale works in the von Martian tradition. In our days, relatively few concise 
floras for tropical regions have been successfully completed and published, and 
some are still marred by awkward formats; apart from the Flora of West Tropical 
Africa, mention can be made of Flora of Java (1963-68), Flowering plants of 
Jamaica, and Tree flora of Malaya (1972+ , still in progress but with good pros- 
pects for early completion). All of these are (or will become) widely-used standard 
works and will be of more real value than many grander but unfinished floras. 


Fisher (1968) has called attention to the proliferation of data which faces 
systematic botanists today. This has had an effect on large-scale independent 
monographic work, particularly in large families (Jacobs, 1969), and it has become 
more convenient in many cases to do this work through the medium of large-scale 
regional or national Floras, there being fewer independent outlets or special 
monographic series than was the case in past decades. Fisher has also drawn atten- 
tion to weaknesses in verbal descriptions, stressing the importance of illustrations; 
this has special relevance to the humid tropics where there are so many different 
kinds of plants to be considered and where the percepticn of most people is much 
more visually than literarily oriented. This point has been clearly recognized by the 
author of such Asian works as Cay-co mien-nam Viét-Nam (Pham, 1970-72), 
Iconographia cormophytorum sinicarum (Anonymous 1972+ ), and Choson 
singmul myongchip (Chong, 1956-57). These are all atlas-floras comprising small 
figures and parallel text, with analytical keys playing a supporting rdle; although 
they are modelled on “‘Western”’ atlas-floras, I believe that something of the Asian 
(and particularly Chinese) botanical tradition has also played a rdle in their 
creation. Some of them are also relatively “‘concise” as Floras, here owing something 
to the traditions of Bentham and his contemporaries. 


Watson (1971) has called for just a return to the Benthamian tradition of 
“concise” Floras, and makes the significant suggestion that the kind of information 
which now tends to go into elaborate ‘archival’? Floras is more appropriate to 
other kinds of taxonomic publication or for storage and retrieval through data 
banks or other non-print media. Believing that the two philosophies of Flora- 
writing — the information/archival and the practical — should be separated and 
that a given work should follow one or the other, Watson considers that many 
Floras are confused in this respect and in the end represent unhappy compromises, 
failing in both areas; they are neither useful sources of comparative data nor 
practical tools for identification (and still expensive!), and have not conceded that 
under present conditions these functions must be virtually separated. He concludes 
by stating that “‘we have all these advantages [computerization, philosophical 
analysis, masses of data, etc.], yet have more difficulty in getting to grips with real 
problems than Bentham did.” 


A step in the direction suggested by Watson was taken by the development 
after 1968 of the FNA Program (Shetler, 1971; Shetler et al., 1973). This was to 
be a relatively sophisticated information storage-and-retrieval system which would 
be linked with a concise conventional flora in some 5-6 volumes in the manner 
of Flora Europaea; the production of a hard-copy flora was viewed in part as a 
recognition of the strength of convention and tradition in Flora-writing. However, 
the project was killed in 1973 as a result of administrative pressures on science 
and internal and external politics; it later became evident that the new methodology 
threatened to become the master rather than the servant of the operation (Shetler, 
1974) and at this writing it is a moot point whether EDP-IR will become a really 


effective tool in Flora-writing in the way hoped for by its advocates. Some smaller — : 


projects are, however, under way, e.g. for Vera Cruz, Mexico (Gémez-Pompa & 
Butanda 1973; G6mez-Pompa & Nevling 1973) and in South Africa (Hall, 1974) © 
and it is these upon which attention will be focused in the years to come. Related 
schemes involve the complete encoding of essential data from the specimens in 


Style of Floras 247 


the Queensland Herbarium at Brisbane and the South African National Herbarium 
at Pretoria; from these it may eventually be possible to produce inter alia preli- 
minary floristic catalogues for these areas. 


FUTURE DEVELOPMENT 


The above references to the introduction of EDP-IR methodology — claimed 
to be the most important change to the philosophies of Flora-writing for a century 
— lead naturally to the final question: what of Floras in the future? The impact 
of new methodologies could eventually bring about the revolution hoped for by 
ap advocates, but firstly some key philosophical (and practical) questions must 

resolved. 


Floras today, as Watson has noted, are often confused in their philosophy and 
are deficient in many ways as a result. Most of them, unless they are really 
elaborate, large-scale works with a consistent format and standard of information 
content, are of little use for comparative data because of the pull of traditional 
essentialist conventions in the writing process; most authors still see identification 
as a principal aim (supplemented by limited information of relatively general 
interest such as habitat, distribution, life-form, phenology and karyotypes) but in 
many cases are obliged, or feel obliged, to include more comprehensive information, 
resulting in a confusion of objectives. Keys are often highly selective, too, and in 
floras where the manual-key format prevails (such as Flora of Java) it becomes 
very difficult to extract useful comparative data. 


What, then, might be the best way to resolve the apparent impasse? Firstly, 
there should be much more effort given in planning new projects to the philosophy 
and objectives of the proposed work as well as to the means, manpower, and 
motivation available (especially for larger works which may take, even in a concise 
form, many years to complete). Secondly, more concern should be given to the 
standardization of data accumulation and organization and the avoidance of the 
losses that occur when work is published. In this, connexion, much depends upon 
continuing improvements in EDP-IR methodology, further introduction of data- 
processing in herbaria and in individual research, and an improved political under- 
standing of the value of such methods in systematic publication (and their limita- 
tions!). 

Personally, I believe that the best role for a Flora as such today remains the 
practical one: inventory, identification and essential related data. To the “‘essential 
data” of Bentham’s time there should now be added that from ecology and karyo- 
logy (cf. van Steenis, 1954) as well as plenty of illustrations. In addition, there 
should be a clear indication of where taxonomic or biosystematic problems occur 
as has been so well handled in Flora of New Zealand by Allan et al. (1961, 1971). 
If lesser-known areas are involved (as is the case with most of the humid tropics), 
it may be desirable to expand supporting data and commentary (including 
citations) somewhat, as is being done with the Flora of Turkey (which, in my 
Opinion, is one of the best of current larger floras dealing with lesser-known areas 
and one very kindred in spirit to the famous ‘‘Kew Series’ of the 19th century). 
In addition, concise floras should always have references to standard monographs, 
revisions, floras and other contributions under each family and genus heading. 


By contrast, large-scale floras should be viewed as having an entirely separate 
function; they should not be undertaken except for large natural regions such as 
Malesia or for very large political entities such as the U.S.S.R. They should 
perhaps even be run as open-ended serials rather than as ‘“‘closed” works, as was 
done with North American Flora some years ago and is being done with Flora 
Neotropica. Furthermore, much of the archival function of such works, with their 


248 Gardens’ Bulletin, Singapore — XX1IX (1976) 


often elaborate synonymy, could be assumed by non-print media and EDP-IR 
systems (as was envisioned by the FNA Program), doing away with the need for 
storing much relatively specialized data in increasingly costly print media; instead, 
such information could be generated in microcard or microfiche form (readers are 
now becoming relatively inexpensive and widespread) or as processed output. 
Detailed information in this form could then be used for the preparation and 
publication in print media of conventional “‘concise” floras (as well as for the 
production of major systematic treatments). 


For some little-known areas where time or local conditions may not permit 
the preparation of more extensive works, I believe it desirable to continue to 
produce annotated enumerations or checklists. These should preferably be in the 
manner of Merrill’s Enumeration of Philippine Flowering Plants, though if keys 
can be added, so much the better. Such a format would have perhaps been the 
best method at the present time for a complete listing of the Papuan flora. An 
excellent example of what can be done in a relatively short time for a comparatively 
little-known areas with limited manpower is Prodromus einer Flora von Siidwesta- 
frika (Merxmiiller et al., 1966-72), previously referred to. There is no room, 
however, for improperly annotated or unannotated checklists. 


In many tropical regions (and developing countries generally) careful conside- 
ration should be given to making the results of systematic botanical work readily 
available to the public — in other words, to the concomitant preparation of works 
which will have a wide impact and can be seen to be useful. Atlas-Floras such as 
those already noted, where most or all species are illustrated, may have a greater 
audience than more conventional works. Keys should be simple and _ practical; 
descriptions should be concise, clear, and provide the essentials (easier if illustrations 
are used consistently). In these areas, it will only be a small number of persons who 
would prefer a detailed treatment, and this could be provided from other sources. 
Where the total flora is very large (and comprehensive works often correspondingly 
costly, especially in local terms), there is also scope for a number of works of more 
limited scope. Thus continuing attention should be given to forest floras and tree 
books (which often have considerable public appeal) as well as works on grasses, 
weeds, etc. One humid tropical country, Malaysia Barat (Malaya), is particularly 
well supplied with such partial works. For teaching purposes, it may often suffice 
to have a compact, illustrated school-manual covering a range of more easily 
accessible species (van Steenis, 1962). One of the finest of tropical manuals ever 
published remains E.J.H. Corner’s Wayside trees of Malaya (2nd ed., 1952); this 
is considered a favourite by my students in New Guinea because of its interesting 
text, many illustrations, and clear keys. This should be revised and updated, and 
more of its kind (there being lamentably few in the tropics) should be written. In 
New Guinea, because the “‘official’ botanists have been interested more in 
specialized, mostly technical floristic works than in books aimed at local people, 
the University Herbarium at Port Moresby has commenced work on a series of 
illustrated teaching booklets on the local flora, each dealing with a given habitat 
or life-form. 


There will certainly be instances where it is necessary or desirable to make 
encyclopaedic information readily available on a given group (or groups) of plants. 
In these cases, this is better done outside the realm of floras, i, as separate 
publications or in serials. The best systematic encyclopaedia ever produced was 
Die natiirlichen Pflanzenfamilien, and it would be highly desirable if the means 
and manpower could be found to complete the second edition of this work or 
undertake a new version in English. However, it should avoid becoming too bogged 
down in detail, a fault shown by the second edition here and there. Much of such 
detail could better be handled by non-taxonomic publications (Heywood, 1973) 
such as Biology and Chemistry of the Umbelliferae. 


Style of Floras 249 


References 
ANON. 1974. Trends, priorities, and needs in systematic and evolutionary biology. 
Syst. Zool, 23: 416-439 (also in Brittonia26: 421-444). 


BENTHAM, G. 1861. Outlines of Botany. In his Flora hong-kongensis, pp. i-xxxvi. 
Reeve & Co., London. 

—_— 1874. On the recent progress and present state of knowledge of 

systematic botany. Rept Brit. Assoc. Adv. Sci. 1847: 27-54. 


BLAKE, S. T. & A. C. ATWOOD. 1942 Geographical guide to the floras of the 
world, I. 336 pp. (U.S.D.A. Misc. Publ, 401.) Washington. 


BRENAN, J. P. M. 1963. The value of floras to underdeveloped countries. Impact 
(Paris). 
DE CANDOLLE, A. 1880. La Phytographie. Masson, Paris. 


DAVIS, P. H. & V. H. HEYWOOD. 1963. Principles of angiosperm taxonomy. 
Oliver & Boyd, Edinburgh & London. 


De WOLF, G. P., Jr. 1963. On the Flora Neotropica. Taxon 12: 251-253. 
1964. On the sizes of floras. Ibid., 13: 149-153. 


FISHER, F. J. F. 1968. The role of geographical and ecological studies in taxonomy, 
In Heywood, V. H. (ed.). Modern methods in plant taxonomy, pp. 241-259. 
Academic Press, London & New York. 


GOMEZ-POMPA, A., and C. A. BUTANDA (eds.) 1973. El uso de computadoras 
en la Flora de Vera Cruz. Instituto de Biologia, Dept. de Botanica, U.N.A.M., 
Mexico City. 

GOMEZ-POMPA, A., and L. I. NEVLING. 1973. The use of electronic data- 
processing methods in the Flora of Veracruz program. Contr. Gray Herb. 203: 
49-64. 

HALL, A. V. 1974. Museum specimen record data storage and retrieval. Taxon 23: 
23-28. 


HEYWOOD, V. H. 1973. Ecological data in practical taxonomy. In his Taxonomy 
and ecology, pp. 329-347. Academic Press, London & New York. 


JACOBS, M. 1969. Large families — not alone! Taxon 18: 253-262. 


LEANDRI, J. 1967. La fin de la dynastie des Jussieu et l’éclipse d’une chaire au 
Muséum (1853 a 1873). Adansonia, n.s. 7: 443-450. 


SHETLER, S. G. 1971. Flora North America as an information system. BioScience 
21: 524, 529-532. 


1974. Demythologizing biological data banking. Taxon 23: 71-100. 


SHETLER, S. G. et al. 1973. A guide for contributors to Flora North America 
(FNA). Provisional ed. 28 pp., appendices (Flora North America Rpt. 65) 
Washington. 


STAFLEU, F. A. 1971. Linnaeus and the Linnaeans, (Regnum Veg. 79.) Utrecht: 
LA.P.T. 


Van STEENIS, C. G. G. J. 1954. General principles in the design of Floras. In 
Huitiéme Congrés International de Botanique, Paris, Rapp. et Comm., sects. 
2,4,5,6, pp. 59-66. Paris. 


250 Gardens’ Bulletin, Singapore — XXIX (1976) 


1962. The school flora as a medium for instruction in the tropics. 
proc. Ninth Pacific Sci, Congr., 4 (Botany): 139-140. 
TAYLOR, R. A. 1971. The Flora North America Project. BioScience 21: 521-523. 


VOSS, E. G. 1952. The history of keys and phylogenetic trees in systematic biology. 
J. Sci. Labs. Denison Univ. 43: 1-25 (quoted from Radford, A.E., et al. 1974. 


Vascular plant systematics, p. 523. Harper & Row, New York). 


WATSON, L. 1971. Basic taxonomic data: the need for organisation over presen- 
tation and accumulation. Taxon 20: 131-136. 


tate ® « 


This World We Live in Will Be Only as Beautiful 
as You and I Make It 


by 


EpwIn A. MENNINGER 
P.O. Box 107, Stuart, Florida 33494, U.S.A. 


The beauty of the landscape might be defined as a visual loveliness that 
excites and exhilarates the senses pleasurably or exalts the mind or spirit. It is not 
necessarily confined to colour, though often augmented or brought out by contrasts 
of light and dark, or emphasized by colourful patterning, or affected by lighting 
displays. The contour of a mountain may be beautiful, or the depth of a yawning 
chasm may awaken a deep and almost overwhelming awe of the magnificence 
spread before the eye. 


But the landscape of man-created communities throughout the world is too 
often lost in a maze of lawns and trees with their predominating blanket of green. 
This uninterrupted sameness is worsened in the warm areas of the earth where 
spring flowers are just a memory and autumn leaf colouring is unknown. 


In Florida where I live and in similar warm areas throughout the world, the 
beauty of our landscape depends solely on how and where brilliant colours are 
utilized to brighten, decorate or emphasize the eye’s acceptance of surroundings 
that are perpetually green. Untold numbers of lakes, waterways, sounds, estuaries, 
and nearly a thousand miles of ocean beaches create unexcelled natural beauty of 
their kind, especially when accentuated with light and shadow with the help of sun 
and moon, and can even achieve a wild sort of beauty with the aid of tempestuous 
winds. Sunrise and sunset provide the only colour overtones in these natural 
surroundings, usually fleeting, often magnificent. But, by and large, the natural 
landscape in Florida is an eternal, unending, unchanging vastness of green with 
nothing but daylight to bring its values to the eye. For without the eye, how can 
there be any physical beauty? There is a spiritual beauty known to all of us, but 
that develops in a world apart from material things and knows neither sunlight 


nor shadow. The physical landscape requires colour to achieve the ultimate in 
beauty. 


Ponce de Leon must have been dreaming when he christened his discovery 
Florida — the land of flowers. There were no flowers, nothing but a vast expanse 
of green. It is easy to understand why people reaching California are overwhelmed 
by “the splendor of poppy fields ablaze in the sun of May.” The gorgeous blue- 
bonnets of Texas are an eye-filling sight at their peak. And even in midsummer on 
the Kansas plains, the sight of the sunflowers, “tawny and gold and brown,”’ is 
more magnificent than many other wild flower colonies. But in Florida, Ponce de 
Leon found no such display because there was none. 

In the south end of the State, where Ponce de Leon never arrived, there are 
two native trees with beautiful flowers — the Geiger tree (Cordia sebestena L.) 
with quantities of burnt-orange blossoms among the evergreen leaves, blooming off 
and on several times a year; and the Lignum Vitae (Guaiacum officinale L.) with 
the richest sky-blue starlike flowers all up and down the branches, a breath-taking 


251 


252 Gardens’ Bulletin, Singapore — XXIX (1976) 


sight. The Geiger tree is sparingly cultivated half way up the state, but the Lignum 
Vitae is too slow growing to be useful as an ornamental and is almost never seen 
out of its native tropics. 


Along the north line of Florida, by the Georgia-Alabama border, two beautiful 
native flowering trees add sparkle to the Jandscape — the Southern Magnolia 
(Magnolia grandiflora L.) and the Fever tree or Maiden’s Blushes (Pinckneya 
pubens Michx) with its gorgeous Rhododendron-like flowers, but Ponce de Leon 
did not see these either. He saw green trees and lots of them. 

Many books are available today with literally thousands of colour photographs 
of the gorgeous flowers to be found in all parts of the world, and available to 
each one of us for our personal experience and enjoyment, if we only make the 
effort. 


B. Y. Morrison, genius of the world of azaleas, long head of the U.S.D.A. 
Bureau of Plant Introduction, and kingpin of the American Horticultural Society 
for many years with both his pen and his purse, wrote the foreword in this author’s 
book on Flowering Trees of the World in which 425 colour plates depict some of 
the most beautiful. Morrison was a dreamer too and he dreamed big. He wrote 
in part: 

“Tt is true, perhaps, that many of the trees shown will be of no value to 

many a reader as plants for his garden, and that some may never even find a 
single place in these United States where they may repeat the miracle of their 
flowering. Does that matter too much? No, a thousand times no, for a mere 
examination of the pictures alone will open one’s eyes to beauty and urge on 
one’s zeal toward new efforts to know and experience, within the possible 
realm of one’s own garden life, things he had never dreamed of. 


“In this day and age, dare one dream? A thousand times yes, for without 
a dream there is no vision, and without vision, the people perish.” 


Hawaii is the classic example of how beauty on the landscape is born in the 
hearts of the people who live there. Like Florida, Hawaii has no native flowering 
trees that are outstandingly beautiful in blossom, except Clermontia and a few 
Hibiscus, and these are seldom seen. Yet the world has come to think of Hawaii 
as the ultimate in floral beauty. Why? Because the beauty which lies in the hearts 
of the Hawaiian people has found expression by the planting of millions of 
beautiful flowering trees which, in a fertile volcanic soil, pour out their spectacular 
flowers in eye-filling displays. The trees that bear them are from other warm 
countries, not from Hawaii. The gorgeous shower trees (Cassia sp.) are native to 
India. The magnificent Plumeria trees (which Floridians insist on calling 
Frangipani”) are natives of Mexico. One Hawaiian garden has 72 kinds of 
Plumeria trees; can you imagine such a spectacle? Some of these have blossoms 
6 inches across! Flowers of Plumeria are particularly useful in making leis because 
they do not wilt when picked. The Hawaiian people hang bouquets around the 
necks of visitors and natives, mix moonlight and the music of steel guitars and 
chorus voices, to convince the guests that here is a flower heaven, We have the 
same moonlight in Florida; all we need is more beauty in our hearts. 


Yes, no doubt about it, Ponce de Leon was dreaming. Four hundred years 
before our time he caught a glimpse of the magnificent spectacle that Florida 
would become when flowers of every size and hue from every warm country on 
earth would come here to make their home and add their beauty and colour to 
an indescribably lovely landscape. He saw the beauty that man could and would 


Facing plate: Tabebuia argentea (Bur. & K. Sch.) Britton from Paraguay. 


ar. tad 


This world we live in 253 


create, and it is this vision of long ago that is gradually taking place on the Florida 
peninsula. Flowering trees by the millions, flowering shrubs undreamed of except 
by Ponce de Leon, flowering vines and untold numbers of groundlings with bright 
blossoms — all these are the details of a landscape that you and I are striving 
to create. 


What matters the location? Be it Florida or England or New Zealand or 
Kenya, the beauty of the landscape is born of the beauty in our hearts and the 
surroundings of each one of us will be, can be, must be magnificent. Each one of 
us should ask ourselves: ‘““What am I doing today to make my home, my city, 
my State more beautiful?” 


iqsoxe to bossibaus aduruta. 2 3 iF 
idetid sltive egailbnuorg Yo i, blolaw bas 23 ott v3 fit 


enivine 218 1 bas voy led’ eqevbasl & Jo -etiaiebs 


ea. Sa 
19 sbROML th of. : 


onl lo god at eet xi Yo 
or od nso 2d fivegs 1 saae 
sbol entob | is jaw: ny 


Offprint from Gardens’ Bulletin X XIX 255-266 (1976) 


Index to Latin names 


Generic and specific names in roman type are synonyms; new names proposed 


in this book are in bold type. 


Acacia, 50, 120, 195 
Acanthaceae, 74-6, 110 
Acanthococcus sp., 59, 61 
Acer, 186 

Actinidiaceae, 186 
Adenium, 75 

Adoxaceae, 184 
Aegilops, 123 

Aeonium, 48 
Aepocereus, 212 


Agathis borneensis, 93 
dammara, 92, 97 (& fig. 9) 


Aglaia sp., 177 


Agaon, 209, 211-2, 218, 227 
paradoxum, 209-10 


Agaonidae, 207, 209, 211-3, 216 218, 222-7 
Agaoninae, 211-2, 218, 222, 227 

Agaonini, 211 

Agaum, 209 

Agavaceae, 179 

Agavoideae, 188 

Agrianisa myrmecoides, 210 

Agropyron, 123 


Agrostistachys borneensis, 176 
sessilifolia, 176 


Aizoaceae, 187 

Akania, 187 

Alfonsiella, 211, 218, 223, 227 
Allexis cauliflora, 179 
Allotriozoon, 211, 218, 227 
Alnus, 110 

Aloe capitata var. cipolinicola, 48 
Alsophila australis, 179 
Alstonia, 22 

Amaryllidaceae, 123 
Amborella, 186 
Amorphophallus, 76 


Anacardiaceae, 68, 96, 131, 161, 163, 175 


Anacardium occidentale, 163 
pumilum, 61 


Ancylanthus rubiginosus, 69 
Andira inermis, 61 
Andryala spp., 50 


Angiospermae, 183 et seq. 
Angylocalyx oligophyllus, 177 
Anisophyllea quangensis, 69 
Anisoptera, 128-9, 132 et seq. 
Anneslea, 109 
Annona stenophylla, 68 
Annonaceae, 68, 90, 96, 132 
Annonales, 186 
Annoniflorae, 184 
Annonineae, 187 
Aploastomata, 211 
Apocrypta, 209, 211-2, 215-fig. 2, 225, 228 
longitarsus, 191, 225 
paradoxa, 209-11 
perplexa, 209-11 
westwoodi, 225 
Apocryptini, 212, 224-fig. 8g-h, 225-6 
A pocry ptophagus, 209 
explorator, 210 
Apocynaceae, 68, 90, 96 
Aporpium caryae, 151 
dimidiatum, 151 et seq. 
hexagonoides, 151 ef seq. 
Arachnoidea, 68 
Araliaceae, 68 
Araucaria, 20, 110 
Arbutus andrachne, 17 
Areciflorae, 187 
Argostemma, 74, 79 
Arisaema, 75 
anomalum, 75 
filiforme, 76 
fimbriatum, 75 
umbrinum, 76 
Armoracia, 123 
Arthrophyllum, 20 
Arthropoda, 112 


Artocarpus, 4, 35 
ser. Angusticarpi, 37 
anisophylla, 37 
sect. Artocarpus, 37 
subg. Artocarpus, 35-6 (& fig. la-e) 
ser. Cauliflori, 37 
sect. Duricarpus, 37 
elasticus, 36 (& fig. 1f), 37-8 
fulvicortex, 36 (& fig. lh-i), 37 
heterophyllus, 16, 35, 37-8 
hispidus, 36 (& fig. la-d) 


255 


256 


ser. Incisfolii, 37 
integer, 35, 37-8 
var. silvestris, 37 
kemando, 37 
lanceifolius, 37 
multifidus, 37 
peltatus, 36 — fig. 1f-g ; 
subg. Pseudojaca, 35-8 (& fig. 1f-i) 
rigidus, 37 
ser. Rugosi, 36-7 
sericicarpus, 37 
spp., 29 
styracifolius, 37 
tamaran, 37 
teysmannii, 37 
Arundo donax, 17 
Aspidium flaccidum, 147 
Aster, 49 
multiflorus, 49 
novae-angliae, 49 
Asteraceae, 187 (see also Compositae) 
Asteridae, 173 
Astragalus, 128 
Austrobaileya, 186 
Avicennia marina, 16 
Baikiaea, 67 
plurijuga, 67 
Balanitoideae, 187 
Balanocarpus, 128 
Balanopaceae, 175 
Balanophora, 106 
Balanops pancheri, 175 
Bambusa arundinacea, 17 
Barbeyaceae, 187 
Barringtonia, 111 
calyptrocalyx, 177 
Begonia, 75-7, 79 
evansiana, 167 (& fig. 7) 
Begoniaceae, 165, 173 
Bencomia, 48 
Bennettitales, 184 
Berberidaceae, 175 
Berberidales, 186 
Bertolonia, 78 
Bertiera simplicicaulis, 178 
Bignoniaceae, 176 
Bikkia macrophylla, 178 
Blackstonia perfoliata 171 (& fig. 10A) 
Blastophaga, 209-12, 214, 215 fig. 1, 217-8, 
227-8 


caricae, 208 

ficus, 208 

grossorum, 207 

javana, 220 

psenes, 208-9, 213-4, 216-20 (& fig. 4), 225-6 
quadraticeps, 214, 220-2 

sycomori, 208 

vaidi, 220 


Blastophaginae, 212, 218, 222, 227 
Boea lanata, 176 


Garden’s Bulletin, Singapore — XX1X (1976) 


Boletales, 155 
Boletellus, 155, 159 
Boletus, 4 
albipurpureus, 159 
amarellus, 159 
ananas, 155 
catervatus, 159 
chrysenteron, 159 
cornalinus, 155 et seq. 
parasiticus, 159 
Phoeniculus, 159 
subg. Phylloporus, 155 et seq. 
‘Piperati’, 155, 159 
porphyrosporus, 159 
pseudorubinellus, 159 
puniceus, 159 
roseolus, 159 
rubinellus, 159 
rubriporus, 159 
rubritubifera, 159 
satisfactus, 159 
strobilaceus, 155 
subtomentosus, 159 
versicolor, 159 
subg. Xerocomus, 155 et seq. 
Bombacaceae, 90, 96, 131 
Bombax, 22 
valetonii, 29 
Bonnetioideae, 187 
Borassus aethiopum, 179 
Brachylaena, 50-1 
neriifolia, 51 
Brachystegia russelliae, 68 
Brackenridgea arenaria, 69 
Brassica, 123 
Brighamia rockii, 176 
Bromeliinae, 187 
Brucea antidysenterica, 178 
Bruineae, 187 
Bupleurum, 48 
Burmannia longifolia, 76 
sphagoides, 76 
Burmaniaceae, 76 
Burseraceae, 90, 96 
Butomaceae, 184 
Byrsonima verbascifolia, 61 
Cactaceae, 48, 123, 187 


Caesalpinia, 111 
pulcherrima, 14 


Calamus sp., 120 
Callicarpa saccata, 120 
Caloncoba suffruticosa, 68 
Calophyllum, 111 
Calycanthaceae, 186 
Calycenthus, 186 


Campanula, 48, 165 
carpatica, 165, pl. 1 opp. 172. 
medium, 165 
rotundifolia, 165, 166 fig. 1 


Index 


Campanulaceae, 42 et seq., 123, 165, 173 
Lobelioideae, 45, 176 


Campanulales, 173 
Campsis, 113 


Campylospermum duparquetianum, 177 
sacleuxii, 177 
subcordatum, 177 
zenkeri, 177 


Canavalia, 111 

Cannaceae, 187 

Canthium, 69 

Caprifoliaceae, 186 

Captaincookia margaretae, 178 

Cardioteris, 186 

Carica papaya, 172 (& fig. 12), 176 
sp., 176 

Caricaceae, 165, 173, 176 

Caricineae, 187 

Carlina, 48 

Caryocar brasiliense subsp. intermedium, 61 

Caryocaraceae, 90, 96, 187 

Caryophyllidae, 173 

Cassia, 59 
floribunda, 170 (& fig. 8A) 

Cassytha, 116 

Casuarina, 111 

Casuarinaceae, 114, 187 

Caulopteris sp., 179 

Caytoniales, 20, 184 

Cecropia, 120-1 

Ceiba pentandra, 29 

Celastraceae, 68, 90, 96 

Celosia cristata, 117 

Celsia, 128 . 

Centrolepidoceae, 187 

Ceratonia, siliqua, 196 (& fig. 4) 

Ceratosolen, 211, 214-5 (& Fig. 2), 218, 225, 
227-8 


arabicus, 191, 194, 201-2, 217 fig. 6, 220-3 
bakeri, 228 

capensis, 223 

coecus, 210 
emarginatus, 220, 228 
flabellatus, 223 
fusciceps, 220 

galili, 223 

hewitti, 220-1 
marshalli, 228 
nanus, 228 

notus, 214, 220 
pygmaeus, 228 


Ceroxylon, 48 
Chalcididae, 209, 211-2 
Chalcidoidea, 212, 216 


Chalcis centrinus, 208 
explorator, 209 
psenes, 208 


Chamaeclitandra henriquesiana, 68 


Chenopodiineae, 187 
Chimonanthus, 186 


Chironia linoides, 171 (& fig. 10B) 


Chisocheton, 20 

macranthus, 177 

medusae, 177 

polyandrus, 177 

princeps, 177 

setosus, 177 
Chlamydocola chlamydantha, 178 
Chloranthaceae, 186 
Chrysanthemum, 48 
Chrysobalanaceae, 68, 90, 187 
Chrysophyllum soboliferum, 61 
Chytranthus longiracemosus, 178 

mangenotii, 178 

pilgerianus, 178 

welwitschii, 178 


Circaea lutetiana, 166 fig. 3A, 168 


Cissus fragilis, 75 
Cistaceae, 165, 173 


Citrus nobilis, 196 (& fig. 4) 
spp., 196 


Clarkia, 115 
Clavaria, 3 


Clavija lancifolia, 179 
longifolia, 179 


Cleidion lasiophyllum, 176 


Clerodendrum, 111 
buchneri, 69 
fistulosum, 120 
lanceolatum, 69 
milne-redheadii, 69 
pusillum, 69 
triplinerve, 69 


Cochlospermaceae, 68 


Cochlospermum insigne, 59, 61 
tinctorium, 68 


Cocos nucifera, 179 
Codiaeum variegatum, 117 
Coffea macrocarpa, 178 


Cola buntingii, 178 
caricaefolia, 178 
mahoundensis, 178 


Colea lantziana, 176 
nana, 176 
sp., 176 


Colubrina, 111 
Combretaceae, 68, 96 


Combretum, 61 
argyrotrichum, 68 
brassiciforme, 68 
harmsianum, 68 
lineare, 68 
paniculatum, 61 
platypetalum, 68 
relictum, 68 
sericeum, 61, 68 
viscosum, 68 


257 


258 


Commelinineae, 187 


Compositae, 42 et seq., 110, 123, 176 
Cichorieae, 49 


Connaraceae, 176, 187 
Jollydoroideae, 187 


Conyza vernonioides, 50 
Cordaitales, 184 


Cordia, 50, 111 
sebestana, 251 


Cornineae, 186 

Cornus mas, 16 
Cosmianthemum, 74 
Cotylanthera, 76 

Cotylelobium, 128-9, 132 et seq. 
Courtella, 209 

Crambe, 48 

‘Crassocephalum’, 46-7 
Critogaster, 223 


Crossogaster, 211-2 
triformis, 223 


Crossosomataceae, 188 
Cruciferae, 123 
Crypteroniaceae, 186 


Cryptosepalum exfoliatum, 68 
maraviense, 68 


Ctenolophon, 110 

Cucumis sativus, 168 
Cucurbitaceae, 96, 129, 168, 171 
Cunonia macrophylla, 176 
Cunoniaceae, 176, 187 

Cussonia corbusieri, 68 


Cyanea aspleniifolia, 176 
carlsonii, 175-6 
giffardii, 176 

Cyathea, 48 
camerooniana, 180 

Cycadaceae, 110 

Cycadeoidea jenneyana, 180 

Cycas, 111 
circinnalis, 21, 180 
revoluta, 180 

Cyclanthaseae, 187 

Cynipidae, 212 

Cynips caricae, 207-8 
cycomori, 207-8 
ficus, 207-8 
psenes, 207-8 
sycomori, 207-8 

Cynopterus brachyotis, 29 

Cyperaceae, 63 

Cyperus, 111 

Cypraea moneta, 200 

Cyrillaceae, 188 


Cyrtandra, 74, 78-9 
mirabilis, 74 
penduliflora, 75 
radiciflora, 74 


Garden’s Bulletin, Singapore — XXIX (1976) 


splendens, 78 

Dacrydium pectinatum, 92-3 
Daphniphyllineae, 186 
Davidsonia, 187 


Decatoma, 226 
fici, 227 


Degeneria, 186 
Deilagaon, 211, 227 


Deinbollia fanshawei, 69 
sp., 178 


Delissea undulata, 176 


Delpydora gracilis, 178 
macrophylla, 178 


Dendriopoterium, 48 
Dendrocacaclia, 51 
Dendrocalamus strictus, 17 
Dendrocnide moroides, 179 
Desmodium, 111 
Diazella, 226 
Dichapetalaceae, 68 . 
Dichapetalum bullockii, 68 
cymosum, 66, 68 
rhodesicum, 68 
Didiereaceae, 187 
Didissandra, 74 
Didymelaceae, 187 
Didymocar pus, 74, 78-9 
gracilipes, 75 
malayanus, 75 
Digitalis, 48 
purpurea, 77 


Dilleniaceae, 68 
Dillenioideae, 186 


Dilleniidae, 173 
Dioncophyllaceae, 187 


Diospyros batocana, 66 
chamaethamnus, 66, 68 
galpinii, 68 
lycioides, 68 
virgata, 68 

Dipsacales, 173 


Dipterocarpaceae, 4, 127 et seq., 186 
Dipterocarpoideae, 128 
Monotoideae, 128, 187 


Dipterocarpus, 128-9, 131 et seq. 
Distyliopsis, 186 

Dodonaea, 111 

Dolichoris, 227 

Doona, 128-9, 132 et seq. 
Dossinia marmorata, 78 
Dracontomelum iianieseiecs 20 
Drosophila, 130 


Dryobalanops, 1289, 132 et seq. 
beccarii, 91-3 


Dryopteris flaccida, 147 


mere 


Index 


Duabanga grandiflora, 29 


Durio, 4, 25-6 
acutifolius, 26 
beccarianus, 26 
dulcis, 26 
grandiflorus, 26 
graveolens, 26, 32 
griffithii, 26 
kutejensis, 26 
lowianus,32 
malaccensis, 26, 32 
oxleyanus, 26 
pinangianus, 26, 32 
testudinarum, 26 
wyatt-smithii, 26 
ziberthinus, 25 et seq. 


Dynatogmus, 223 
Dypsis hildebrandtii, 179 
Dysoxylum urens, 177 
Ebenaceae, 68 
Echeverioideae, 188 
Echinodermata, 112 
Echium spp., 48, 50 
Ehretia, 50 

Eisenia, 211 

Ekebergia pumila, 68 
Elaeis guineensis, 179 
Elaeocarpaceae, 21, 186 
Elatostema, 74 


Elephantorrhiza elephantina, 66, 68 
obliqua, 66, 68 
woodii, 68 


Elisabethiella, 211, 218, 223, 227 
Elymus, 123 

Embolanthera, 186 
Encephalartos laurentinus, 180 


Endospermum, 22 
spp., 120 


Entada dolichorrhachis, 68 
nana, 68 


Eonycteris spelaea, 25, 29 
Eospermatopteris, sp., 180 
Epacridaceae, 187 

Epichrysomallinae, 210, 212, 226, 227 
Epilobium angustifolium, 166 fig. 2B, 168 
Episcia reptans, 78 

Epithema, 77 

Ericaceae, 123, 165, 170, 173, 186 
Ericales, 173 

Eriobotrya japonica, 196 fig. 4 
Eriocaulineae, 187 

Eriogonoideae, 188 

Eryngium spp., 

Erysimum, 48 


Erythrina, 111 
baumii, 59, 68 
zeyheri, 66, 68 


Escallonioideae, 187 

Espeletia spp., 42, 50-1 
spicata, 176 

Eucalyptus, 61 

Euclea crispa, 59, 60 fig. 1, 68 

Eudecatoma, 226 

Eudecatominae, 210 2,12, 226 


Eugenia angolensis, 69 
capensis, 69 
pusilla, 66, 69 

Eujacobsenia, 226 

Eukoebelea, 224-5 

Euphorbia, 111 
ankarensis, 176 
bupleurifolia, 176 
lophogona, 176 
moratii, 176 
spp., 48 


Euphorbiaceae, 90, 96, 176 
Euphorbiales, 187 
Eupomatia, 186 
Eupristina, 211, 218, 227 
Eurycoma longifolia, 178 
Eurytomidae, 210, 212 
Fagaceae, 132 

Fagales, 186 


Ficus, 4, 13, 46, 57, 122-3, 130, 186 
sect. Adenosperma, 227-8 
alba, 214 
sect. Americana, 223, 225, 227 
ampelas, 226 
auriculata, 213, 220, 228 
sect. Auriculosperma, 228 
benghalensis, 13, 15, 209 
capensis, 223 


259 


carica, 16, 196 fig. 4, 197, 199, 203, 207-9, 


213-7 (& fig. 1), 219-20, 223 
sect. Conosycea, 225-7 
costaricana, 220, 222 
dammaropsis, 228 
sect. Ficus, 220, 227-8 
subg. Ficus, 209, 220, 225-8 
fistulosa, 214, 220-1 
sect. Galoglychia, 226-7 
hemsleyana, 220, 222 
hirta, 213, 220 
hispida, 220 
sect. Kalosyce, 227 
sect. Leucogyne, 227 
macrophylla, 214, 220 
sect. Malvanthera, 223, 226-7 
mauritiana, 209 
monahasae, 228 
sect. Neomorphe, 225, 227-8 
nota, 214-220 
oligodon, 228 
sect. Oreosycea, 226-8 
sect. Papuasycea, 228 
sect. Pharmacosycea, 220, 225, 227 
subg. Pharmacosycea, 227 
subsect. Pomifera, 228 
pritchardii, 228 
pseudopalma, 228 
ser. Pseudopalmae, 228 


260 


pungens, 228 
Pygmaea, 69 
racemosa, 220, 228 


religiosa, 196 (& fig. 4), 220, 223 


sect. Rhizocladus, 227 
ser. Rivulares, 228 
rivularis, 228 

roxburghii, 213 
rubiginosa, 214 
salicifolia, 223 

sect. Sinosycidium, 227 
spp., 195, 214, 217-20, 222, 227 
sect. Stilpnophyllum, 227 
sect. Sycidium, 226-8 
sect, Sycocarpus, 225-8 


sycomorus, 191 et seq., 207, 209, 211, 215 


fig. 2, 220-1, 223-225 


subg. Sycomorus, 209, 220, 223, 225-8 


terragona, 209 
theophrastoides, 177 
tinctoria, 226 

var. gibbosa, 226 
tseila, 220 
tuerckheimii, 223 
sect. Urostigma, 226 


subg. Urostigma, 209, 220, 225-8 


verruculosa, 69 
virens, 220, 227 


Fimbristylis, 111 


Flacourtiaceae, 68, 96, 165, 171, 173, 176 


Fouquieriaceae, 188 

Freycinetia, 137 

Fuchsia fulgens, 166 fig. 2A, 167 
Gaertnera, 109 

Galbulimima, 186 

Ganosoma, 224 

Garcinia buchneri, 68 


Gardenia conferta, 178 
subacaulis, 69 


Garrya, 186 
Garryaceae, 188 


Gentianaceae, 165, 171, 173 
Gentianoideae, 49 


Gentianales, 173 
Geraniales, 173, 187 
Geraniaceae, 176 
Geranium canariense, 176 
Gerrardanthus, 75 


Gesneriaceae, 76-8, 123, 176 
Cyrtandroideae, 186 


Ginkgo, 110 

Goethea strictiflora, 177 
Gomphostemma, 74 
Goniogaster, 211 
Gonostylus, 186 
Goodeniaceae, 187 


Gossypium, 16, 114 
arboreum, 114 
thurberi, 114 

Goupia, 187 


Garden’s Bulletin, Singapore — XXIX (1976) 


Gramineae, 123 
Micrairoideae, 187 


Grasseiana, 226 


Grewia decemovulata, 69 
falcistipula, 69 
herbacea, 69 


Grias sp., 177 
Guaiacum officinale, 251 
Guarea richardiana, 177 
Guettarda, 111 
Guttiferae, 68, 90, 96 
Gyrostemonaceae, 187 
Haemodoreae, 187 
Hagiophyton sp., 179 
Haloragaceae, 187 
Hamamelidales, 186 
Hamamelidae, 173 
Hammelidiflorae, 184 
Hamamelidoideae, 186 
Haplostomata, 211, 212 
Harmsiopanax, 19-20 
Harpephyllum caffrum, 175 
Hectorelloideae, 184 


Hedychium, 75, 76 
cylindricum, 76 


Hedysarum, 44 

Heeria nitida, 68 

Heliciopsis, 20 
Heliconioideae, 187 

Hericium coralloides, 159 
Hernandia, 111 

Herrania albiflora, 178 
Heterandrium, 223 
Heterocentron roseum, 170 (& fig. 8B) 
Hexacorallia, 112 

Hibiscus, 111 

Hicksbeachia pinnatifolia, 178 
Hippuridaceae, 184 

Hopea, 128-9, 132 et seq. 
Hoplestigmataceae, 187 
Hordeum spontaneum, 198 


Houmiriaceae, 90, 96 
Houmirioideae, 187 


Hoya, 120 

Huacaceae, 187 

Hugonia gossweileri, 68 
Hydnophytum, 120 
Hydnoraceae, 187 
Hldrocaryaceae, 165, 173 
Hy poxidoideae, 187 
Icacinaceae, 96 


Ichneumon psenes, 208 
ficarius, 208 


Idarnella caricae, 208 


t 
3 


Index 


Idarnes, 209, 211, 224-5 
carme, 209-10 
orientalis, 210 
pteromaliodes, 210 
stabilis, 210 
transiens, 210 

Idarninae, 211-2 

Idarnodes caricae, 208 
ficarius, 208 

Idarnomorpha, 209 

Idiospermum, 186 

Ilex, 110 

Illiciineae, 186 

Impatiens duthieae, 75 
flanaganae, 75 
mirabilis, 75 

Ingonia digitata, 178 

Insecta, 112 

Ipomoea, 111 


Iridaceae, 187 
Geosiridoideae, 187 


Isanisa decatomoides, 210 

Ischaemum, 111 

Isoglossa, 75 

Ixonanthaceae, 68 

Jacaranda decurrens, 61 

Jagera serrata, 178 

Jambosa acris, 177 

Jollydora duparquetiana, 176 

Juglandineae, 186 

Julianella, 211 

Juncaceae, 187 

Knema, 21 

Knightia, 110 

Korthalsia, 120 

Kradibia, 211 

Labiatae — Prostantheroideae, 187 

Landolphia gossweileri, 68 

Lannea edulis, 68 
gossweileri, 68 


Katangensis, 68 

virgata, 68 
Lastrea dayi, 148 

flaccida, 147 

gracilescens var. decipiens, 147 
Lauraceae, 90, 96, 116, 132, 176 
Laurus nobilis, 16 
Lecythidaceae, 68, 90, 96, 177 

Lecythidoideae, 187 

Napoleonoideae, 187 

Planchonioideae, 186 


Leguminosae, 90, 96, 111, 131, 165, 170, 173 


Caesalpinioideae, 68, 187 

Mimosoideae, 68, 177 187 

Papilionoideae, 68, 177 
Leptactina benguelensis, 69 
Licania dealbata, 61 


Limonium, 48 


Linaceae, 68 

Linariantha, 74 
Biporrhopalum, 211, 218, 227-8 
Lipothymus, 226 
Lissocarpaceae, 187 

Litsea ripidion, 176 


Loasa, 168 
vulcanica, 167 (& fig. 4), pl. 2 opp. 172 


Loasaceae, 165, 168, 173, 187 
Lobelia, 22, 41 et seg., 165 


assurgens, 50 
bambuseti, 45, 49 
deckenii, 45, 46 


subsp. keniensis, 45 


dortmanna, 51 

giberroa, 45, 49 

subsect. Haynaldianae, 45 et seq. 
nicotianifolia, 45, 47 

subsect. Nicotianifoliae, 45 et seq. 
nubigena, 45 


rhynchopetalum, 41 fig. 1, 45, 47, 49 


sect. Rhynchopetalum, 42 et seq. 
subsect. Rueellianae, 45 et seq. 
stricklandiae, 167 

sumatrana, 45, 46 

telekii, 45, 46 

urens, 50 

wollastonii, 45, 49-50 


Lodoicea maldavica, 179 
Loganiaceae, 68 
Loranthaceae, 114 

Luffa cylindrica, 168 
Lupinus alopecuroides, 48 
Lyginopteris oldhamia, 180 
Lythraceae, 165, 173 
Macadamia angustifolia, 178 
Macrothelypteris, 145 et seq. 


multiseta, 149 
torresiana, 148-9 


Magnistipula sapinii, 68 
Magnolia grandiflora, 252 
Magnoliacease, 186 
Magnoliidae, 173 
Magnoliineae, 186 
Mahonia bealei, 175 
Maingaya, 186 
Malpighiaceae, 68 
Malvaceae, 114, 177 
Malvales, 173 

Mangifera indica, 16, 161 et seq. 
Maniella, 227 


delhiensis, 220 


Mapania, 78 
Marantaceae, 187 
Marcgraviaceae, 187 
Marquesia, 128 
Martyniaceae, 187 
Mastixiodendron, 109 


261 


262 


Matthiola incana, 16 
Mauritia flexuosa, 179 
Medeola, 73 
Medullosa noei, 180 
Medusagynaceae, 187 
Megaphyton sp., 179 


Melastomataceae, 49, 120, 165, 173 
Astronioideae, 186 
Chitonoideae, 188 


Melia azedarach, 196, 196 fig. 4 
Meliaceae, 68, 131, 177 
Melianthaceae, 187 
Menispermaceae, 177 
Mentzelia gronoviifolia, 168 
lindleyi, 168 (& fig. 5) 
Mercurialis, 73 
Metasequoia, 110 


Metathelypteris, 145 
dayi, 146, 148 
decipiens, 145-7 
flaccida, 145-7 
fragilis, 146 


Metroxylon, 20 


Micranisa, 210 
pteromaloides, 210 


Mikaniopsis, 50 
Mimulopsis, 75 
Mimusops schimperi, 199 
Miscogasteridae, 212 
Monimiaceae, 109, 186 
Monodontomerinae, 212 


Monophyllaea, 77, 116 
glauca, 78 


Monoporandra, 128, 129, 132 et seq. 
Monotes, 128 
Montinioideae, 187 
Moraceae, 35, 69, 90, 96, 177 
Morinda, 111, 116 

angloensis, 69 


Morus alba, 196 fig. 4 
nigra, 196 fig. 4 


Musa, 16 
Musaceae, 187 
Myosotis, 50 


Myristicaceae, 21-2, 90, 96 
Myrmecodia, 120-1 
Myrsinaceae, 177 


Myrtaceae, 69, 90, 96, 177 
Leptospermoideae, 187 


Myrtales, 173 
Myzodendraceae, 184 
Napoleona gossweileri, 68 
Naucleeae, 116 
Neckia, 74 

serrata, 179 


Garden's Bulletin, Singapore — X XIX (1976) 


Nectarinia johnstonii johnstonii, 44 
Neostrearia, 186 


Neosycophila, 212-3 
omeomorpha, 226 


Nepenthaceae, 186 
Nepenthes, 117, 120 


Nephrodium dayi, 148 
gracilescens var. decipiens, 147 
singalanense, 148 


Nigeriella, 218, 227 
Nolina recurvata, 179 
Nothofagus, 110 
Nyctaginaceae, 96 
Nymphaeles, 186 
Nypa, 110 

Obetia radula, 179 


Ochna confusa, 69 
katangensis, 69 
leptoclada, 69 
macroculyx 69 
manikensis, 69 
mossambicensis, 69 
pygmaea, 69 
richardsiae, 69 
schweinfurthiana, 62 


Ochnaceae, 69 
Ochthocosmus candidus, 68 
Octocorallia, 112 
Octomeles, 22 
Oenocarpus distichus, 179 
Olacaceae, 90, 96 

Olea europaea, 16 
Oleaceae, 114 

Oliniaceae, 187 
Onagraceae, 165, 167, 173 
Oncostemon sp., 177 


Orchidaceae, 117, 121 
A postasioideae, 186 
Cy pripedioideae, 186 


Oriolus oriolus, 200 
Oroxylon indicum, 29 
Ostrearia, 186 

Otitesella, 209, 212-3 
Otitesellini, 211-3, 226 
Otomys orestes orestes, 44 
Oxera coriacea, 179 
Oxytropis, 128 
Pachynocarpus, 128 
Pachypodium, 48 
Pachystigma pygmaeum, 69 
Paenaeaceae, 187 
Palaeocycas integer, 180 
Palmae, 73, 96, 179 
Pandanaceae, 73, 137, 179, 186 


Index 263 


Pandanales, 137 sect. Paralophostigma, 140 
subsect. Parvi, 141 
Pandanus, 4, 111, 137 et seq. sect. Perrya, 140 
sect. Acanthostyla, 141, 138 sect. Platyphylla, 141 
sect. Acrostigma, 141 princeps, 179 
subg. Acrostigma, 141 sect. Pseudoacrostigma, 141 
subsect. Acrostigma, 141 sect. Pulvinistigma, 141 
subsect. Alticolae, 141 subsect. Pumili, 141 
sect. Asterodontia, 140 sect. Rykia, 140 
sect. Asterostigma, 140 subg. Rykia, 140 
sect. Athrostigma, 141 subsect. Rykia, 140 
subsect. Atrodentata, 140 sect. Rykiella. 141 
sect. Australibrassia, 141 sect. Rykiopsis, 140 
subsect. Austrokeura, 141 subsect. Scabridi, 141 
sect. Barklya, 141 subsect. Semikeura, 141 


sect. Barrotia, 140 
sect. Bernardia, 140 
subsect. Bidens, 140 
sect. Brongniartia, 140 sect. Souleyetia, 141 
subsect. Calcicola, 140 subsect. Souleyetia, 141 
sect. Cauliflora, 138, 140 spiralis, 137, 140 

sect. Cheilostigma, 140 sect. Stephanostigma, 141 
sect. Coronata, 141 subsect. Sussea, 141 


sect. Seychellea, 141 
sigmoideus, 138 
sect. Solmsia, 140 


subg. Coronata, 141 sect. Tridens, 138, 140 
sect. Cristata, 141 sect. Utilissima, 141 
sect. Curvifolia, 141 sect. Veillonia, 140 


danckelmannianus, 179 
sect. Dauphinensia, 141 
subsect. Dimissistyli, 141 


sect. Vinsonia, 141 
subg. Vinsonia, 141 


subsect. Elaphrocarpus, 141 Paphagus, 209 

sect. Elmeria, 141 sidero, 209 

sect. Epiphytica, 141 Paphiopedilum, 78 
oe Parakoebelea, 209, 224-5 


sec. Eydouxia, 141 
sect. Fagerlindia, 141 Rettig cs 

sect. Foullioya, 141 Parapristina, 227 

sect. Fusiforma, 141 Parashorea, 128-9, 132 et seq. 
subsect. Glaucophyllae, 141 P hia. 226 

subsect. Gressitia, 140 pepe haan 


sect. Heterostigma, 141 Parinari, 67 

sect. Hombronia, 140 capensis, 59, 63-6 (& fig. 3), 68 
subsect. Insulanus, 141 curatellifolia, 59, 66 

sect. Intraobtutus, 141 obtusifolia, 61 

sect. Involuta, 141 Paris. 73. 108 

sect. Jeanneretia, 141 Sari 

sect. Kaida, 140 Parkia, 29 

sect. Kanehiraea, 141 Paropsia brazzeana, 69 


sect. Karuka, 140 : 
sect. Kurzia, 141 Passiflora quadrangularis, 171 


subg. Kurzia, 141 Passifloraceae, 69, 171 


sect. iam 140 Pavetta pygmaea, 69 
sect. Lonchostigma, 141 : 
sect. Lophostigma, 140 Pedaliaceae, 187 


subg. Lophostigma, 140 Pegoscapus, 211, 218, 222-3, 225, 227 
subsect. Malaya, 140 estherae, 220, 222 
sect. Mammilarisia, 141 tonduzi, 220, 222 


sect. Marginata, 141 


sect. Martellidendron, 141 Pellicieroideae, 187 


subg. Martellidendron, 140 Penianthus sp., 177 

sect. Maysops, 140 

sect. Megakeura, 141 Pentacme, ‘ay 132 

sect. Megastigma, 140 ‘Pentacorallia’, 112 

sect. Metamaysops, 140 Pentagonia gigantifolia, 178 


sect. Microstigma, 141 


subsect. Multispina, 140 Peridiscus, 187 


; sect. Mydiophylla, 140 Petasites, 51 

subsect. Ornati, 141 Phaseolus. 170 
sect. Pandanus ‘ 
subg. Pandanus, 141 Phegopteris, 145 et seq. 
subsect. Pandanus, 141 pyrrhorhachis, 150 


subsect. Papilionatae, 141 Phoenix dactylifera, 196 fig. 4 


264 


Philotrypesini, 212, 224 fig. 8e-f, 225 


Philotry pesis, 212, 226, 228 
caricae, 208, 210, 213, 216, 217 fig. 5, 218 
longicauda, 208 
transiens, 210 


Phragmites australis, 17 
Phyllanthus, 59 

Phyllobotryon spathulatum, 171 (& fig. 11) 176 
Phylloporus rhodoxanthos, 159 
Physothorax, 212, 223 
Phytelephas macrocarpa, 179 
Pinckneya pubens, 252 
Pinaceae, 116 

Pithecellobium hansemannii 
Pittosporaceae, 178 
Pittosporineae, 187 
Pittosporum ceratii, 178 
Placodiscus bancoensis, 178 
Planchonella pronyensis, 178 
Platanus, 113 

Platyneura testacea, 209 


Playtyscapa, 211-2 
frontalis, 209-10 


Pletocomia, 19 


Pleistodontes, 211, 214, 218, 222, 227 
froggatti, 213-4, 220, 222 
imperialis, 214, 222 


Plesiostigma, 212 
Podophyllum, 73 
Podostemaceae, 187 
Poinciana pulcherrima, 14 
Polanisa lutea, 210 
Polemoniaceae, 188 
Polygalineae, 187 
Polygonaceae, 76 
Coccoloboideae, 187 
Polygonum, 29 
Polypodium, 146 
brunneum, 150 
paludosum, 149 
phegopteris, 146 
rectangulare, 149 
Polystichum torresianum, 148 
Pongamia, 111 
Pontederiaceae, 187 
Porphyrellus porphyrosporus, 159 
Prainea, 35, 38 
Primula vulgaris, 77 
Prionastomata, 211 


Protea, 63 
angolensis, 69 
heckmanniana, 69 
madiensis, 63 
paludosa, 69 
trichophylla, 69 


Proteaceae, 69, 114, 178, 187 


Garden’s Bulletin, Singapore — XXIX (1976) 


Prunus persica, 196 fig. 4 
Psaronius sp., 179 
Pseuderanthemum, 74 

Pseudidarnes, 223 
Pseudomantalania macrophylla, 178 


Pseudophegopteris, 145 et seq. 
aurita, 149-50 
paludosa, 149-50 
rectangularis, 149-50 


Psidium guajava, 196 fig. 4, 197 
Psorospermum mechowii, 68 
Psychotria spp., 69 
Pteridospermae, 184 

Pteropus vampyrus, 29 

Punica granatum, 196 fig. 4 


Puya, 48, 51 
ramondii, 48 


Pycnocoma angustifolia, 176 


Pygmaeothamnus concrescens, 69 
zeyheri, 69 


Pyrus communis, 196 fig. 4 


Quercus, 110 
ilex, 16 


Quiinaceae, 187 

Radlkofera calodendron, 178 
Rafflesia, 106 

Rafflesioideae, 186 

Ranales, 109 

Rapanea grandiflora, 177 
Raphanus, 123 

Rauvolfia nana, 68 

Resia, 75 

Restionaceae, 187 
Rhabdodendraceae, 187 
Rhamnaceae, 69 

Rheum nobile, 48 
Rhizophora mucronata, 16 
Rhizophoraceae, 69, 111, 186 
Rhododendron ponticum, 170 


Rhus diversiloba, 163 
glabra, 163 
kirkii, 68 

Richetia, 128 


Rosaceae, 90, 96, 121 
Pomoideae, 114 


Rosales, 173 

Rosidae, 173 

Rousettus aegyptiacus, 192, 193 fig. 1, 195-6, 
198 


stekelesi, 198 
Roystonea oleracea, 179 


Rubiaceae, 69, 76, 96, 109, 123, 165, 178 
Henriquesioideae, 187 
Ruellia, 78 


Index 


Rutaceae, 186 
Dictyolomatoideae, 187 
Spathelioideae, 187 


Rutiflorae, 184 
Sabiaceae, 186 


Salacia bussei, 68 
kraussii, 68 


luebbertii, 68 
Sapindaceae, 69, 96, 131, 178 
Sapotaceae, 90, 96, 132, 178, 187 
Sapotineae, 187 
Sararanga, 137 
Sarcolaenaceae, 187 
Sarraceniaceae, 187 
Saussurea gossipiphora, 48 
Scaevola, 111 
Schinus, 163 
Scrophulariaceae, 117, 123 
Scytopetaliceae, 187 
Scytopetalineae, 187 
Secundeisenia, 211 
Selaginella, 78 


Semecarpus magnifica, 175 
sp., 175, pl. 1 opp. 176 


Senecio, 22, 41 et seq. 
asperulus, 50 
bonariensis, 50 
brassica, 43-4, 46 
sect. Crociserides, 44 et seq. 


subg. Dendrosenecio, 42 et seq. 


gigas, 43 
hypargyraeus, 50 
johnstonii, 43 
subsp. barbatipes, 43-4 
subsp. refractisquamatus, 43 
keniodendron, 43-4, 50 
leucadendron, 43 
mannii, 21, 43, 47 
maranguensis, 50 
redivivus, 43 
Senecioneae, 45 
Seres, 226 
Shorea, 128-9, 132 et seq. 
albida, 92-3 


Simaroubaceae, 96, 131, 178 
Alvaradoideae, 187 
Kirkioideae, 187 


Sloanea, 21 
Solanaceae, 178, 187 
Solanum, 116 

aff. Solanum, 178 
Sonchus, 48-9 


Sonerila, 74, 79 
borneensis, 78 
tenuifolia, 78 


Sonneratia, 111 


Sophora, 111 
sp., 177 


Sparganiaceae, 137 
Sparmannia africana, 170 
Sphaerosepalaceae, 187 
Sphedothamnus angolensis, 68 
Spilanthes, 111 

Spondias, 163 
Stackhousiaceae, 187 
Staphyleaceae, 186 
Staurogyne, 76 

Steenisia, 75 

Stemona, 108 

Stemonoporus, 128-9 
Sterculiaceae, 178 
Streptocarpus molweniensis, 77 


Strobilanthes, 75 
cernuus, 75 
kunthianus, 75 


Strobilomyces, 155 
Strophanthus angusii, 68 
Strychnos gossweileri, 68 
Stylidiaceae, 165, 173 


Stylidium graminifolium, 168 (& fig. 6) 


Sycobia bethyloides, 210 
Sycobiomorphella, 226 


Sycocrypta, 209, 211 
croeca, 209-10 


Sycoecini, 211-3, 226 
Sycolacides, 211-2 


265 


Sycophaga, 209, 211-2, 215 fig. 2, 223, 225, 228 


crassipes, 208 
paradoxa, 210 


sycomori, 191, 202, 208, 211, 223-5 


Sycophagides, 211-2 
Sycophaginae, 210-3 


Sycophagini, 211-2, 223-5 (& fig. 8a-b) 


Sycophila, 212, 226-7 
decatomoides, 210 


Sycophilomorpha, 226 


Sycoryctini, 209, 212, 224-6 (& fig. 8c-d) 


Sycoscapter stabilis, 210 
Sycoscapteridea, 214, 225 
Symplocaceae, 178, 186 


Symplocos, 110 
stravadioides, 178 


Syzygium guineense subsp. huillense, 69 


Tabebuia argentea, pl. opp. 252 
Tacazzea, 75 
Tamarindus indica, 17 


Tapeinosperma pachycaulum, 177 


cristobalense, 177 
sp., 177 


Tapiphyllum spp., 69 


Tecophilaeaceae-Cynastroideae, 187 


Terminalia, 21, 22, 111 
mollis, 63 


266 Garden's Bulletin, Singapore — XXIX (1976) 


Ternstroemia, 144 
bancana, 144 
corneri, 143 et seq. 
penangiana, 144 
wallichiana, 144 
Tetracera masuiana, 68 
Tetrachondroideae, 184 
Tetragonaspis, 209 
Tetrameles, 22 
Tetrapus, 211-2, 218, 222-3, 227 
spp., 220 
Thalassiophyta, 3 
Thamnopteria schlectendahlii, 180 
Theaceae, 4, 109, 143 
Theiflorae, 184 
Thelypteridaceae, 145 et seq. 
Thelypteris, 145 
brunnea, 149-50 
decipiens, 147 
flaccida, 147 
oppositipinna, 149 
paludosa, 149 
singalanensis, 148 


torresiana, 148 
uliginosa, 148 


* Theobroma mariae, 178 


Theophrastaceae, 179, 187 


Tiliaceae, 69, 165, 170, 173 
Neotessmannioideae, 187 
Tetralicoideae, 187 


Torymidae, 209-11, 226 

Toryminae, 212, 223 

Tournefortia, 111 

Trechus, 45 

Tremellales, 4, 151 

Tricalysia cacondensis, 69 
suffruticosa, 69 

Trichilia quadrivalvis, 64 (& fig. 3), 65, 68 

Trichoscypha ferruginea, 175 

Trimeniaceae, 186 

Tristania, 109 


Triticum, 123 
boeoticum, 198 
dicoccum, 198 
monococcum, 198 


Tropaeolaceae, 165, 170, 173 


Tropaeolum minus, 170 (& fig. 9) 
Typhaceae, 137 

Typhales, 137 

Umbelliferae, 76, 121 

Uncaria, 116 


Upuna, 128 
borneensis, 128 


Urticaceae, 179 

Valentinella, 211 

Valeriana officinalis, 166 fig. 3B, 168 
Valerianaceae, 165, 173 

Vateria, 128-9 132 et seq. 

Vatica, 128-30, 132 et seq. 
Vellozioideae, 187 

Verbascum, 128 


Verbenaceae, 69, 179 
Chloanthoideae, 179 


Verschaffeltia splendida, 179 
Viola, 165 


Violaceae, 96, 165, 173, 179 
Leonioideae, 187 


Violales, 173 
Vochysiaceae, 96 
Walkerella temeraria, 210 


Waterstoniella, 209, 211, 218, 222, 227 
frontalis, 210 
masii, 222 


W edelia, 111 

Welwitschia, 42 

Whiteodendron moultonianum, 93 
Williamsonia sewardiana, 180 
Winteraceae, 186-7 

Xanthorrhoea spp., 48 
Xanthorrhoideae, 187 


Xerocomus macrobbii, 159 
nothofagi, 159 
rufostipulatus, 159 

Xerospermum intermedium, 19 

Yucca brevifolia, 51 
spp., 48 

Zingiberaceae, 74, 186 

Ziziphus jujuba, 16 
spina-christi, 196 
zeyherana, 69 


ERRATA 


In the running head of pages 15 to 266, 1976 should read 1977 
p. 25, in abstract line 10 from bottom for dehiscense read dehiscence 
pp. 27, 29, 31, 33, in running head, for Zibethinus read zibethinus 
p. 61, line 7, for et al read et al. 
p. 64, line 5 for C. De, read C.DC 
p. 70, line 8, for Act. a read Acta 
line 9, for 3: (1) read 3 (1). 
p. 79, for MOORE, H.J. read MOORE, H.E. 


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